Hostname: page-component-7b9c58cd5d-v2ckm Total loading time: 0 Render date: 2025-03-15T19:29:59.105Z Has data issue: false hasContentIssue false
  • English
  • Français

Nucleases: diversity of structure, function and mechanism

Published online by Cambridge University Press:  21 September 2010

Wei Yang
Wei Yang*
Affiliation:
Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, 9000 Rockville Pike, Bldg. 5, Rm B1-03, Bethesda, MD 20892, USA
*
*Author for correspondence: W. Yang, Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, 9000 Rockville Pike, Bldg. 5, Rm B1-03, Bethesda, MD 20892, USA.Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Nucleases cleave the phosphodiester bonds of nucleic acids and may be endo or exo, DNase or RNase, topoisomerases, recombinases, ribozymes, or RNA splicing enzymes. In this review, I survey nuclease activities with known structures and catalytic machinery and classify them by reaction mechanism and metal-ion dependence and by their biological function ranging from DNA replication, recombination, repair, RNA maturation, processing, interference, to defense, nutrient regeneration or cell death. Several general principles emerge from this analysis. There is little correlation between catalytic mechanism and biological function. A single catalytic mechanism can be adapted in a variety of reactions and biological pathways. Conversely, a single biological process can often be accomplished by multiple tertiary and quaternary folds and by more than one catalytic mechanism. Two-metal-ion-dependent nucleases comprise the largest number of different tertiary folds and mediate the most diverse set of biological functions. Metal-ion-dependent cleavage is exclusively associated with exonucleases producing mononucleotides and endonucleases that cleave double- or single-stranded substrates in helical and base-stacked conformations. All metal-ion-independent RNases generate 2′,3′-cyclic phosphate products, and all metal-ion-independent DNases form phospho-protein intermediates. I also find several previously unnoted relationships between different nucleases and shared catalytic configurations.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 44 , Issue 1 , February 2011 , pp. 1 - 93
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

13. References

Abelson, J., Trotta, C. R. & Li, H. (1998). tRNA splicing. Journal of Biological Chemistry 273, 12685–12688.Google Scholar
Adams, P. L., Stahley, M. R., Kosek, A. B., Wang, J. & Strobel, S. A. (2004). Crystal structure of a self-splicing group I intron with both exons. Nature 430, 45–50.Google Scholar
Aizawa, Y., Xiang, Q., Lambowitz, A. M. & Pyle, A. M. (2003). The pathway for DNA recognition and RNA integration by a group II intron retrotransposon. Molecular Cell 11, 795–805.Google Scholar
Akutsu, A., Masaki, H. & Ohta, T. (1989). Molecular structure and immunity specificity of colicin E6, an evolutionary intermediate between E-group colicins and cloacin DF13. Journal of Bacteriology 171, 6430–6436.CrossRefGoogle Scholar
Allemand, F., Mathy, N., Brechemier-Baey, D. & Condon, C. (2005). The 5S rRNA maturase, ribonuclease M5, is a Toprim domain family member. Nucleic Acids Research 33, 4368–4376.Google Scholar
Altermark, B., Smalas, A. O., Willassen, N. P. & Helland, R. (2006). The structure of Vibrio cholerae extracellular endonuclease I reveals the presence of a buried chloride ion. Acta Crystallographica D: Biological Crystallography 62, 1387–1391.CrossRefGoogle Scholar
Andersen, K. R., Jonstrup, A. T., Van, L. B. & Brodersen, D. E. (2009). The activity and selectivity of fission yeast Pop2p are affected by a high affinity for Zn2+ and Mn2+ in the active site. RNA 15, 850–861.Google Scholar
Andrade, J. M., Pobre, V., Silva, I. J., Domingues, S. & Arraiano, C. M. (2009). The role of 3′–5′ exoribonucleases in RNA degradation. Progress in Molecular Biology and Translation Sciences 85, 187–229.CrossRefGoogle Scholar
Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science 181, 223–230.Google Scholar
Aravind, L. (1999). An evolutionary classification of the metallo-beta-lactamase fold proteins. In Silico Biology 1, 69–91.Google Scholar
Aravind, L. & Koonin, E. V. (1998). A novel family of predicted phosphoesterases includes Drosophila prune protein and bacterial RecJ exonuclease. Trends in Biochemical Sciences 23, 17–19.Google Scholar
Aravind, L., Leipe, D. D. & Koonin, E. V. (1998). Toprim – a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Research 26, 4205–4213.CrossRefGoogle Scholar
Arcus, V. L., Backbro, K., Roos, A., Daniel, E. L. & Baker, E. N. (2004). Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. Journal of Biological Chemistry 279, 16471–16478.Google Scholar
Ariyoshi, M., Vassylyev, D. G., Iwasaki, H., Nakamura, H., Shinagawa, H. & Morikawa, K. (1994). Atomic structure of the RuvC resolvase: a Holliday junction-specific endonuclease from E. coli. Cell 78, 1063–1072.Google Scholar
Arni, R. K., Watanabe, L., Ward, R. J., Kreitman, R. J., Kumar, K. & Walz, F. G. Jr. (1999). Three-dimensional structure of ribonuclease T1 complexed with an isosteric phosphonate substrate analogue of GpU: alternate substrate binding modes and catalysis. Biochemistry 38, 2452–2461.Google Scholar
Artymiuk, P. J., Ceska, T. A., Suck, D. & Sayers, J. R. (1997). Prokaryotic 5′–3′ exonucleases share a common core structure with gamma-delta resolvase. Nucleic Acids Research 25, 4224–4229.Google Scholar
Avey, H. P., Boles, M. O., Carlisle, C. H., Evans, S. A., Morris, S. J., Palmer, R. A., Woolhouse, B. A. & Shall, S. (1967). Structure of ribonuclease. Nature 213, 557–562.Google Scholar
Baldwin, E. P., Martin, S. S., Abel, J., Gelato, K. A., Kim, H., Schultz, P. G. & Santoro, S. W. (2003). A specificity switch in selected cre recombinase variants is mediated by macromolecular plasticity and water. Chemistry and Biology 10, 1085–1094.Google Scholar
Baldwin, G. S., Waley, S. G. & Abraham, E. P. (1979). Identification of histidine residues that act as zinc ligands in beta-lactamase II by differential tritium exchange. Biochemical Journal 179, 459–463.CrossRefGoogle Scholar
Ban, C. & Yang, W. (1998a). Crystal structure and ATPase activity of MutL: implications for DNA repair and mutagenesis. Cell 95, 541–552.Google Scholar
Ban, C. & Yang, W. (1998b). Structural basis for MutH activation in E. coli mismatch repair and relationship of MutH to restriction endonucleases. EMBO Journal 17, 1526–1534.CrossRefGoogle Scholar
Barabas, O., Ronning, D. R., Guynet, C., Hickman, A. B., Ton-Hoang, B., Chandler, M. & Dyda, F. (2008). Mechanism of IS200/IS605 family DNA transposases: activation and transposon-directed target site selection. Cell 132, 208–220.Google Scholar
Bechhofer, D. H. (2009). Messenger RNA decay and maturation in Bacillus subtilis. Progress in Molecular Biology and Translation Sciences 85, 231–273.Google Scholar
Beese, L. S. & Steitz, T. A. (1991). Structural basis for the 3′–5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO Journal 10, 25–33.Google Scholar
Beloglazova, N., Brown, G., Zimmerman, M. D., Proudfoot, M., Makarova, K. S., Kudritska, M., Kochinyan, S., Wang, S., Chruszcz, M., Minor, W., Koonin, E. V., Edwards, A. M., Savchenko, A. & Yakunin, A. F. (2008). A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. Journal of Biological Chemistry 283, 20361–20371.Google Scholar
Benedik, M. J. & Strych, U. (1998). Serratia marcescens and its extracellular nuclease. FEMS Microbiology Letters 165, 1–13.Google Scholar
Bennett, R. J., Dunderdale, H. J. & West, S. C. (1993). Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion. Cell 74, 1021–1031.CrossRefGoogle Scholar
Bhagwat, M., Hobbs, L. J. & Nossal, N. G. (1997). The 5′-exonuclease activity of bacteriophage T4 RNase H is stimulated by the T4 gene 32 single-stranded DNA-binding protein, but its flap endonuclease is inhibited. Journal of Biological Chemistry 272, 28523–28530.Google Scholar
Bhat, A. G., Leelaram, M. N., Hegde, S. M. & Nagaraja, V. (2009). Deciphering the distinct role for the metal coordination motif in the catalytic activity of Mycobacterium smegmatis topoisomerase I. Journal of Molecular Biology 393, 788–802.Google Scholar
Biertümpfel, C., Yang, W. & Suck, D. (2007). Crystal structure of T4 endonuclease VII resolving a Holliday junction. Nature 449, 616–620.Google Scholar
Biswas, T., Aihara, H., Radman-Livaja, M., Filman, D., Landy, A. & Ellenberger, T. (2005). A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 435, 1059–1066.Google Scholar
Bitinaite, J., Wah, D. A., Aggarwal, A. K. & Schildkraut, I. (1998). FokI dimerization is required for DNA cleavage. Proceedings of the National Academy of Sciences USA 95, 10570–10575.Google Scholar
Blanco, M. G., Matos, J., Rass, U., Ip, S. C. & West, S. C. (2010). Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S. cerevisiae. DNA Repair (Amsterdam) 9, 394–402.Google Scholar
Bork, P. & Sander, C. (1993). A hybrid protein kinase-RNase in an interferon-induced pathway? FEBS Letters 334, 149–152.Google Scholar
Brautigam, C. A. & Steitz, T. A. (1998). Structural principles for the inhibition of the 3′–5′ exonuclease activity of Escherichia coli DNA polymerase I by phosphorothioates. Journal of Molecular Biology 277, 363–377.Google Scholar
Brautigam, C. A., Sun, S., Piccirilli, J. A. & Steitz, T. A. (1999). Structures of normal single-stranded DNA and deoxyribo-3′-S-phosphorothiolates bound to the 3′–5′ exonucleolytic active site of DNA polymerase I from Escherichia coli. Biochemistry 38, 696–704.Google Scholar
Breyer, W. A. & Matthews, B. W. (2000). Structure of Escherichia coli exonuclease I suggests how processivity is achieved. Nature Structural Biology 7, 1125–1128.Google Scholar
Brouns, S. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J., Snijders, A. P., Dickman, M. J., Makarova, K. S., Koonin, E. V. & Van Der Oost, J. (2008). Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960–964.Google Scholar
Brucet, M., Querol-Audi, J., Serra, M., Ramirez-Espain, X., Bertlik, K., Ruiz, L., Lloberas, J., Macias, M. J., Fita, I. & Celada, A. (2007). Structure of the dimeric exonuclease TREX1 in complex with DNA displays a proline-rich binding site for WW domains. Journal of Biological Chemistry 282, 14547–14557.Google Scholar
Buckle, A. M. & Fersht, A. R. (1994). Subsite binding in an RNase: structure of a barnase-tetranucleotide complex at 1·76-A resolution. Biochemistry 33, 1644–1653.Google Scholar
Budd, M. E., Choe, W. & Campbell, J. L. (2000). The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. Journal of Biological Chemistry 275, 16518–16529.Google Scholar
Bujnicki, J. M. (2001). Understanding the evolution of restriction–modification systems: clues from sequence and structure comparisons. Acta biochimica Polonica 48, 935–967.Google Scholar
Bunting, K. A., Roe, S. M., Headley, A., Brown, T., Savva, R. & Pearl, L. H. (2003). Crystal structure of the Escherichia coli dcm very-short-patch DNA repair endonuclease bound to its reaction product-site in a DNA superhelix. Nucleic Acids Research 31, 1633–1639.Google Scholar
Buttner, K., Wenig, K. & Hopfner, K. P. (2005). Structural framework for the mechanism of archaeal exosomes in RNA processing. Molecular Cell 20, 461–471.Google Scholar
Buttner, S., Eisenberg, T., Carmona-Gutierrez, D., Ruli, D., Knauer, H., Ruckenstuhl, C., Sigrist, C., Wissing, S., Kollroser, M., Frohlich, K. U., Sigrist, S. & Madeo, F. (2007). Endonuclease G regulates budding yeast life and death. Molecular Cell 25, 233–246.Google Scholar
Callaghan, A. J., Grossmann, J. G., Redko, Y. U., Ilag, L. L., Moncrieffe, M. C., Symmons, M. F., Robinson, C. V., Mcdowall, K. J. & Luisi, B. F. (2003). Quaternary structure and catalytic activity of the Escherichia coli ribonuclease E amino-terminal catalytic domain. Biochemistry 42, 13848–13855.Google Scholar
Callaghan, A. J., Marcaida, M. J., Stead, J. A., Mcdowall, K. J., Scott, W. G. & Luisi, B. F. (2005). Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437, 1187–1191.Google Scholar
Callebaut, I., Moshous, D., Mornon, J. P. & De Villartay, J. P. (2002). Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family. Nucleic Acids Research 30, 3592–3601.Google Scholar
Calvin, K. & Li, H. (2008). RNA-splicing endonuclease structure and function. Cell Mol Life Sci 65, 1176–1185.Google Scholar
Calvin, K., Xue, S., Ellis, C., Mitchell, M. H. & Li, H. (2008). Probing the catalytic triad of an archaeal RNA splicing endonuclease. Biochemistry 47, 13659–13665.Google Scholar
Carr, S., Walker, D., James, R., Kleanthous, C. & Hemmings, A. M. (2000). Inhibition of a ribosome-inactivating ribonuclease: the crystal structure of the cytotoxic domain of colicin E3 in complex with its immunity protein. Structure 8, 949–960.Google Scholar
Carte, J., Wang, R., Li, H., Terns, R. M. & Terns, M. P. (2008). Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes and Development 22, 3489–3496.Google Scholar
Castillo-Acosta, V. M., Ruiz-Perez, L. M., Yang, W., Gonzalez-Pacanowska, D. & Vidal, A. E. (2009). Identification of a residue critical for the excision of 3′-blocking ends in apurinic/apyrimidinic endonucleases of the Xth family. Nucleic Acids Research 37, 1829–1842.Google Scholar
Cerritelli, S. M. & Crouch, R. J. (2009). Ribonuclease H: the enzymes in eukaryotes. FEBS Journal 276, 1494–1505.Google Scholar
Ceschini, S., Keeley, A., Mcalister, M. S., Oram, M., Phelan, J., Pearl, L. H., Tsaneva, I. R. & Barrett, T. E. (2001). Crystal structure of the fission yeast mitochondrial Holliday junction resolvase Ydc2. EMBO Journal 20, 6601–6611.Google Scholar
Ceska, T. A., Sayers, J. R., Stier, G. & Suck, D. (1996). A helical arch allowing single-stranded DNA to thread through T5 5′-exonuclease. Nature 382, 90–93.Google Scholar
Champoux, J. J. (2001). DNA topoisomerases: structure, function, and mechanism. Annual Review of Biochemistry 70, 369–413.Google Scholar
Champoux, J. J. & Schultz, S. J. (2009). Ribonuclease H: properties, substrate specificity and roles in retroviral reverse transcription. FEBS Journal 276, 1506–1516.Google Scholar
Chanfreau, G., Noble, S. M. & Guthrie, C. (1996). Essential yeast protein with unexpected similarity to subunits of mammalian cleavage and polyadenylation specificity factor (CPSF). Science 274, 1511–1514.Google Scholar
Chang, J. H., Kim, J. J., Choi, J. M., Lee, J. H. & Cho, Y. (2008). Crystal structure of the Mus81–Eme1 complex. Genes and Development 22, 1093–1106.CrossRefGoogle Scholar
Changela, A., Digate, R. J. & Mondragon, A. (2001). Crystal structure of a complex of a type IA DNA topoisomerase with a single-stranded DNA molecule. Nature 411, 1077–1081.Google Scholar
Chapados, B. R., Hosfield, D. J., Han, S., Qiu, J., Yelent, B., Shen, B. & Tainer, J. A. (2004). Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair. Cell 116, 39–50.Google Scholar
Chatterjee, D. K., Hammond, A. W., Blakesley, R. W., Adams, S. M. & Gerard, G. F. (1991). Genetic organization of the KpnI restriction–modification system. Nucleic Acids Research 19, 6505–6509.Google Scholar
Chen, D. S., Herman, T. & Demple, B. (1991). Two distinct human DNA diesterases that hydrolyze 3′-blocking deoxyribose fragments from oxidized DNA. Nucleic Acids Research 19, 5907–5914.Google Scholar
Chen, W. J., Lai, P. J., Lai, Y. S., Huang, P. T., Lin, C. C. & Liao, T. H. (2007a). Probing the catalytic mechanism of bovine pancreatic deoxyribonuclease I by chemical rescue. Biochemical and Biophysical Research Communications 352, 689–696.Google Scholar
Chen, W. J. & Liao, T. H. (2006). Structure and function of bovine pancreatic deoxyribonuclease I. Protein and Peptide Letters 13, 447–453.Google Scholar
Chen, X., Li, N. & Ellington, A. D. (2007b). Ribozyme catalysis of metabolism in the RNA world. Chemistry and Biodiversity 4, 633–655.Google Scholar
Chen, Y., Narendra, U., Iype, L. E., Cox, M. M. & Rice, P. A. (2000). Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Molecular Cell 6, 885–897.Google Scholar
Chen, Y. C., Shipley, G. L., Ball, T. K. & Benedik, M. J. (1992). Regulatory mutants and transcriptional control of the Serratia marcescens extracellular nuclease gene. Molecular Microbiology 6, 643–651.Google Scholar
Cheng, C., Kussie, P., Pavletich, N. & Shuman, S. (1998). Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92, 841–850.Google Scholar
Cheng, Y. & Patel, D. J. (2004). Crystallographic structure of the nuclease domain of 3′hExo, a DEDDh family member, bound to rAMP. Journal of Molecular Biology 343, 305–312.Google Scholar
Chi, Y. I., Martick, M., Lares, M., Kim, R., Scott, W. G. & Kim, S. H. (2008). Capturing hammerhead ribozyme structures in action by modulating general base catalysis. PLoS Biology 6, e234.Google Scholar
Chowdhury, D., Beresford, P. J., Zhu, P., Zhang, D., Sung, J. S., Demple, B., Perrino, F. W. & Lieberman, J. (2006). The exonuclease TREX1 is in the SET complex and acts in concert with NM23-H1 to degrade DNA during granzyme A-mediated cell death. Molecular Cell 23, 133–142.Google Scholar
Christianson, D. W. (1991). Structural biology of zinc. Advances in Protein Chemistry 42, 281–355.Google Scholar
Chu, C. Y. & Rana, T. M. (2007). Small RNAs: regulators and guardians of the genome. Journal of Cellular Physiology 213, 412–419.Google Scholar
Ciccia, A., Mcdonald, N. & West, S. C. (2008). Structural and functional relationships of the XPF/MUS81 family of proteins. Annual Review of Biochemistry 77, 259–287.Google Scholar
Clissold, P. M. & Ponting, C. P. (2000). PIN domains in nonsense-mediated mRNA decay and RNAi. Current Biology 10, R888–890.Google Scholar
Cochrane, J. C. & Strobel, S. A. (2008). Catalytic strategies of self-cleaving ribozymes. Accounts of Chemical Research 41, 1027–1035.Google Scholar
Coleman, J. E. (1992). Structure and mechanism of alkaline phosphatase. Annual Review of Biophysics and Biomolecular Structure 21, 441–483.Google Scholar
Condon, C., Brechemier-Baey, D., Beltchev, B., Grunberg-Manago, M. & Putzer, H. (2001). Identification of the gene encoding the 5S ribosomal RNA maturase in Bacillus subtilis: mature 5S rRNA is dispensable for ribosome function. RNA 7, 242–253.Google Scholar
Correll, C. C., Yang, X., Gerczei, T., Beneken, J. & Plantinga, M. J. (2004). RNA recognition and base flipping by the toxin sarcin. Journal of Synchrotron Radiation 11, 93–96.Google Scholar
Cowan, J. A. (2002). Structural and catalytic chemistry of magnesium-dependent enzymes. Biometals 15, 225–235.Google Scholar
Crow, Y. J., Hayward, B. E., Parmar, R., Robins, P., Leitch, A., Ali, M., Black, D. N., Van Bokhoven, H., Brunner, H. G., Hamel, B. C., Corry, P. C., Cowan, F. M., Frints, S. G., Klepper, J., Livingston, J. H., Lynch, S. A., Massey, R. F., Meritet, J. F., Michaud, J. L., Ponsot, G., Voit, T., Lebon, P., Bonthron, D. T., Jackson, A. P., Barnes, D. E. & Lindahl, T. (2006a). Mutations in the gene encoding the 3′–5′ DNA exonuclease TREX1 cause Aicardi–Goutieres syndrome at the AGS1 locus. Nature Genetics 38, 917–920.Google Scholar
Crow, Y. J., Leitch, A., Hayward, B. E., Garner, A., Parmar, R., Griffith, E., Ali, M., Semple, C., Aicardi, J., Babul-Hirji, R., Baumann, C., Baxter, P., Bertini, E., Chandler, K. E., Chitayat, D., Cau, D., Dery, C., Fazzi, E., Goizet, C., King, M. D., Klepper, J., Lacombe, D., Lanzi, G., Lyall, H., Martinez-Frias, M. L., Mathieu, M., Mckeown, C., Monier, A., Oade, Y., Quarrell, O. W., Rittey, C. D., Rogers, R. C., Sanchis, A., Stephenson, J. B., Tacke, U., Till, M., Tolmie, J. L., Tomlin, P., Voit, T., Weschke, B., Woods, C. G., Lebon, P., Bonthron, D. T., Ponting, C. P. & Jackson, A. P. (2006b). Mutations in genes encoding ribonuclease H2 subunits cause Aicardi–Goutieres syndrome and mimic congenital viral brain infection. Nature Genetics 38, 910–916.Google Scholar
Crow, Y. J. & Rehwinkel, J. (2009). Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Human Molecular Genetics 18, R130–R136.Google Scholar
Cymerman, I. A., Obarska, A., Skowronek, K. J., Lubys, A. & Bujnicki, J. M. (2006). Identification of a new subfamily of HNH nucleases and experimental characterization of a representative member, HphI restriction endonuclease. Proteins 65, 867–876.Google Scholar
Daiyasu, H., Osaka, K., Ishino, Y. & Toh, H. (2001). Expansion of the zinc metallo-hydrolase family of the beta-lactamase fold. FEBS Letters 503, 1–6.Google Scholar
Datta, S., Larkin, C. & Schildbach, J. F. (2003). Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Structure 11, 1369–1379.Google Scholar
Davies, D. R., Goryshin, I. Y., Reznikoff, W. S. & Rayment, I. (2000). Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289, 77–85.Google Scholar
Davies, D. R., Interthal, H., Champoux, J. J. & Hol, W. G. (2004). Explorations of peptide and oligonucleotide binding sites of tyrosyl-DNA phosphodiesterase using vanadate complexes. Journal of Medicinal Chemistry 47, 829–837.Google Scholar
Davies, D. R., Mushtaq, A., Interthal, H., Champoux, J. J. & Hol, W. G. (2006). The structure of the transition state of the heterodimeric topoisomerase I of Leishmania donovani as a vanadate complex with nicked DNA. Journal of Molecular Biology 357, 1202–1210.Google Scholar
De La Sierra-Gallay, I. L., Pellegrini, O. & Condon, C. (2005). Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z. Nature 433, 657–661.Google Scholar
De Silva, U., Choudhury, S., Bailey, S. L., Harvey, S., Perrino, F. W. & Hollis, T. (2007). The crystal structure of TREX1 explains the 3′ nucleotide specificity and reveals a polyproline II helix for protein partnering. Journal of Biological Chemistry 282, 10537–10543.Google Scholar
Declais, A. C. & Lilley, D. M. (2008). New insight into the recognition of branched DNA structure by junction-resolving enzymes. Current Opinion in Structural Biology 18, 86–95.Google Scholar
Demple, B. & Harrison, L. (1994). Repair of oxidative damage to DNA: enzymology and biology. Annual Review of Biochemistry 63, 915–948.Google Scholar
Desai, N. A. & Shankar, V. (2003). Single-strand-specific nucleases. FEMS Microbiology Reviews 26, 457–491.Google Scholar
Deshpande, R. A. & Shankar, V. (2002). Ribonucleases from T2 family. Critical Reviews in Microbiology 28, 79–122.Google Scholar
Deutscher, M. P. & Li, Z. (2001). Exoribonucleases and their multiple roles in RNA metabolism. Progress in Nucleic Acid Research and Molecular Biology 66, 67–105.Google Scholar
Deutscher, M. P., Marshall, G. T. & Cudny, H. (1988). RNase PH: an Escherichia coli phosphate-dependent nuclease distinct from polynucleotide phosphorylase. Proceedings of the National Academy of Sciences USA 85, 4710–4714.Google Scholar
Devos, J. M., Tomanicek, S. J., Jones, C. E., Nossal, N. G. & Mueser, T. C. (2007). Crystal structure of bacteriophage T4 5′ nuclease in complex with a branched DNA reveals how flap endonuclease-1 family nucleases bind their substrates. Journal of Biological Chemistry 282, 31713–31724.Google Scholar
Diaz, R. L., Alcid, A. D., Berger, J. M. & Keeney, S. (2002). Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation. Molecular and Cellular Biology 22, 1106–1115.Google Scholar
Diebler, H., Eigen, M., Ilgenfritz, G., Maass, G. & Winkler, R. (1969). Kinetics and mechanisms of reactions of main group metal ions with biological carriers. Pure Applied Chemistry 20, 93–115.Google Scholar
Dillingham, M. S. & Kowalczykowski, S. C. (2008). RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiology and Molecular Biology Reviews 72, 642–671, Table of Contents.Google Scholar
Domanico, P. L. & Tse-Dinh, Y. C. (1991). Mechanistic studies on E. coli DNA topoisomerase I: divalent ion effects. Journal of Inorganic Biochemistry 42, 87–96.Google Scholar
Dominski, Z. (2007). Nucleases of the metallo-beta-lactamase family and their role in DNA and RNA metabolism. Critical Reviews in Biochemistry and Molecular Biology 42, 67–93.Google Scholar
Dong, B., Niwa, M., Walter, P. & Silverman, R. H. (2001). Basis for regulated RNA cleavage by functional analysis of RNase L and Ire1p. RNA 7, 361–373.Google Scholar
Dong, K. C. & Berger, J. M. (2007). Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450, 1201–1205.Google Scholar
Doudna, J. A. & Cech, T. R. (2002). The chemical repertoire of natural ribozymes. Nature 418, 222–228.Google Scholar
Dryden, D. T., Murray, N. E. & Rao, D. N. (2001). Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Research 29, 3728–3741.Google Scholar
Duan, X., Gimble, F. S. & Quiocho, F. A. (1997). Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity. Cell 89, 555–564.Google Scholar
Duppatla, V., Bodda, C., Urbanke, C., Friedhoff, P. & Rao, D. N. (2009). The C-terminal domain is sufficient for endonuclease activity of Neisseria gonorrhoeae MutL. Biochemical Journal 423, 265–277.Google Scholar
Dyda, F., Hickman, A. B., Jenkins, T. M., Engelman, A., Craigie, R. & Davies, D. R. (1994). Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266, 1981–1986.CrossRefGoogle Scholar
Dziembowski, A., Lorentzen, E., Conti, E. & Seraphin, B. (2007). A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nature Structural and Molecular Biology 14, 15–22.Google Scholar
Eberle, A. B., Lykke-Andersen, S., Muhlemann, O. & Jensen, T. H. (2009). SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nature Structural and Molecular Biology 16, 49–55.Google Scholar
Ebihara, A., Yao, M., Masui, R., Tanaka, I., Yokoyama, S. & Kuramitsu, S. (2006). Crystal structure of hypothetical protein TTHB192 from Thermus thermophilus HB8 reveals a new protein family with an RNA recognition motif-like domain. Protein Science 15, 1494–1499.CrossRefGoogle ScholarPubMed
Eckstein, F. (1985). Nucleoside phosphorothioates. Annual Review of Biochemistry 54, 367–402.Google Scholar
Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A. & Nagata, S. (1998). A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43–50.Google Scholar
Falvey, E., Hatfull, G. F. & Grindley, N. D. (1988). Uncoupling of the recombination and topoisomerase activities of the gamma delta resolvase by a mutation at the crossover point. Nature 332, 861–863.Google Scholar
Farazi, T. A., Juranek, S. A. & Tuschl, T. (2008). The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135, 1201–1214.Google Scholar
Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E. R., Tissier, A., Coulon, S., Dong, M. Q., Ruse, C., Yates, J. R. 3RD, Russell, P., Fuchs, R. P., Mcgowan, C. H. & Gaillard, P. H. (2009). Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138, 78–89.Google Scholar
Fekete, R. A. & Frost, L. S. (2000). Mobilization of chimeric oriT plasmids by F and R100-1: role of relaxosome formation in defining plasmid specificity. Journal of Bacteriology 182, 4022–4027.Google Scholar
Ferre-D'amare, A. R., Zhou, K. & Doudna, J. A. (1998). Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567–574.Google Scholar
Fersht, A. R. & Daggett, V. (2002). Protein folding and unfolding at atomic resolution. Cell 108, 573–582.Google Scholar
Fiedler, T. J., Vincent, H. A., Zuo, Y., Gavrialov, O. & Malhotra, A. (2004). Purification and crystallization of Escherichia coli oligoribonuclease. Acta Crystallographica D: Biological Crystallography 60, 736–739.Google Scholar
Flaherty, K. M., Mckay, D. B., Kabsch, W. & Holmes, K. C. (1991). Similarity of the three-dimensional structures of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proceedings of the National Academy of Sciences USA 88, 5041–5045.Google Scholar
Flick, K. E., Jurica, M. S., Monnat, R. J. JR. & Stoddard, B. L. (1998). DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature 394, 96–101.Google Scholar
Fogg, J. M., Kvaratskhelia, M., White, M. F. & Lilley, D. M. (2001). Distortion of DNA junctions imposed by the binding of resolving enzymes: a fluorescence study. Journal of Molecular Biology 313, 751–764.Google Scholar
Fontecilla-Camps, J. C., De Llorens, R., Le Du, M. H. & Cuchillo, C. M. (1994). Crystal structure of ribonuclease A.d(ApTpApApG) complex. Direct evidence for extended substrate recognition. Journal of Biological Chemistry 269, 21526–21531.Google Scholar
Frazao, C., Mcvey, C. E., Amblar, M., Barbas, A., Vonrhein, C., Arraiano, C. M. & Carrondo, M. A. (2006). Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110–114.Google Scholar
Freemont, P. S., Friedman, J. M., Beese, L. S., Sanderson, M. R. & Steitz, T. A. (1988). Cocrystal structure of an editing complex of Klenow fragment with DNA. Proceedings of the National Academy of Sciences USA 85, 8924–8928.Google Scholar
Friedhoff, P., Franke, I., Meiss, G., Wende, W., Krause, K. L. & Pingoud, A. (1999). A similar active site for non-specific and specific endonucleases. Nature Structural Biology 6, 112–113.Google Scholar
Friedhoff, P., Kolmes, B., Gimadutdinow, O., Wende, W., Krause, K. L. & Pingoud, A. (1996). Analysis of the mechanism of the Serratia nuclease using site-directed mutagenesis. Nucleic Acids Research 24, 2632–2639.Google Scholar
Fukui, K., Nishida, M., Nakagawa, N., Masui, R. & Kuramitsu, S. (2008). Bound nucleotide controls the endonuclease activity of mismatch repair enzyme MutL. Journal of Biological Chemistry 283, 12136–12145.Google Scholar
Gabel, H. W. & Ruvkun, G. (2008). The exonuclease ERI-1 has a conserved dual role in 5·8S rRNA processing and RNAi. Nature Structural and Molecular Biology 15, 531–533.Google Scholar
Gan, J., Shaw, G., Tropea, J. E., Waugh, D. S., Court, D. L. & Ji, X. (2008). A stepwise model for double-stranded RNA processing by ribonuclease III. Molecular Microbiology 67, 143–154.Google Scholar
Gan, J., Tropea, J. E., Austin, B. P., Court, D. L., Waugh, D. S. & Ji, X. (2006). Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 124, 355–366.Google Scholar
Garcin, E. D., Hosfield, D. J., Desai, S. A., Haas, B. J., Bjoras, M., Cunningham, R. P. & Tainer, J. A. (2008). DNA apurinic–apyrimidinic site binding and excision by endonuclease IV. Nature Structural and Molecular Biology 15, 515–522.Google Scholar
Genschel, J., Bazemore, L. R. & Modrich, P. (2002). Human exonuclease I is required for 5′ and 3′ mismatch repair. Journal of Biological Chemistry 277, 13302–13311.Google Scholar
Gerlt, J. A., Coderre, J. A. & Mehdi, S. (1983). Oxygen chiral phosphate esters. Advances in Enzymology and Related Areas of Molecular Biology 55, 291–380.Google Scholar
Ghosh, K., Guo, F. & Van Duyne, G. D. (2007a). Synapsis of loxP sites by Cre recombinase. Journal of Biological Chemistry 282, 24004–24016.Google Scholar
Ghosh, M., Meiss, G., Pingoud, A. M., London, R. E. & Pedersen, L. C. (2007b). The nuclease a-inhibitor complex is characterized by a novel metal ion bridge. Journal of Biological Chemistry 282, 5682–5690.Google Scholar
Glavan, F., Behm-Ansmant, I., Izaurralde, E. & Conti, E. (2006). Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO Journal 25, 5117–5125.Google Scholar
Gomis-Ruth, F. X. & Coll, M. (2006). Cut and move: protein machinery for DNA processing in bacterial conjugation. Current Opinion in Structural Biology 16, 744–752.Google Scholar
Gorchakova, G. A. (1981). [Polynucleotide phosphorylase from rat liver nuclei. Determination of the activity and some properties]. Biokhimiia 46, 797–801.Google Scholar
Gorman, M. A., Morera, S., Rothwell, D. G., De La Fortelle, E., Mol, C. D., Tainer, J. A., Hickson, I. D. & Freemont, P. S. (1997). The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO Journal 16, 6548–6558.Google Scholar
Gottlin, E. B., Rudolph, A. E., Zhao, Y., Matthews, H. R. & Dixon, J. E. (1998). Catalytic mechanism of the phospholipase D superfamily proceeds via a covalent phosphohistidine intermediate. Proceedings of the National Academy of Sciences USA 95, 9202–9207.Google Scholar
Graille, M., Mora, L., Buckingham, R. H., Van Tilbeurgh, H. & De Zamaroczy, M. (2004). Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO Journal 23, 1474–1482.Google Scholar
Grazulis, S., Manakova, E., Roessle, M., Bochtler, M., Tamulaitiene, G., Huber, R. & Siksnys, V. (2005). Structure of the metal-independent restriction enzyme BfiI reveals fusion of a specific DNA-binding domain with a nonspecific nuclease. Proceedings of the National Academy of Sciences USA 102, 15797–15802.Google Scholar
Griffith, J. P., Kim, J. L., Kim, E. E., Sintchak, M. D., Thomson, J. A., Fitzgibbon, M. J., Fleming, M. A., Caron, P. R., Hsiao, K. & Navia, M. A. (1995). X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12–FK506 complex. Cell 82, 507–522.Google Scholar
Grindley, N. D., Whiteson, K. L. & Rice, P. A. (2006). Mechanisms of site-specific recombination. Annual Review of Biochemistry 75, 567–605.Google Scholar
Guarne, A., Ramon-Maiques, S., Wolff, E. M., Ghirlando, R., Hu, X., Miller, J. H. & Yang, W. (2004). Structure of the MutL C-terminal domain: a model of intact MutL and its roles in mismatch repair. Embo Journal 23, 4134–4145.Google Scholar
Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. (1983). The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849–857.Google Scholar
Guo, F., Gopaul, D. N. & Van Duyne, G. D. (1997). Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389, 40–46.Google Scholar
Habraken, Y., Sung, P., Prakash, L. & Prakash, S. (1993). Yeast excision repair gene RAD2 encodes a single-stranded DNA endonuclease. Nature 366, 365–368.Google Scholar
Habraken, Y., Sung, P., Prakash, L. & Prakash, S. (1994). A conserved 5′ to 3′ exonuclease activity in the yeast and human nucleotide excision repair proteins RAD2 and XPG. Journal of Biological Chemistry 269, 31342–31345.CrossRefGoogle Scholar
Hadden, J. M., Déclais, A.-C., Carr, S. B., Lilley, D. M. J. & Phillips, E. V. (2007). The structural basis of Holliday junction resolution. Nature 449, 621–624.Google Scholar
Hale, S. P., Poole, L. B. & Gerlt, J. A. (1993). Mechanism of the reaction catalyzed by staphylococcal nuclease: identification of the rate-determining step. Biochemistry 32, 7479–7487.Google Scholar
Hamdan, S., Carr, P. D., Brown, S. E., Ollis, D. L. & Dixon, N. E. (2002). Structural basis for proofreading during replication of the Escherichia coli chromosome. Structure 10, 535–546.Google Scholar
Harding, M. M. (1999). The geometry of metal-ligand interactions relevant to proteins. Acta Crystallographica D: Biological Crystallography 55, 1432–1443.Google Scholar
Hare, S., Gupta, S. S., Valkov, E., Engelman, A. & Cherepanov, P. (2010). Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464, 232–236.Google Scholar
Harrington, J. J. & Lieber, M. R. (1994). The characterization of a mammalian DNA structure-specific endonuclease. EMBO Journal 13, 1235–1246.Google Scholar
Haruki, M., Tsunaka, Y., Morikawa, M., Iwai, S. & Kanaya, S. (2000). Catalysis by Escherichia coli ribonuclease HI is facilitated by a phosphate group of the substrate. Biochemistry 39, 13939–13944.Google Scholar
Hennecke, F., Kolmar, H., Brundl, K. & Fritz, H. J. (1991). The vsr gene product of E. coli K-12 is a strand- and sequence-specific DNA mismatch endonuclease. Nature 353, 776–778.Google Scholar
Hernick, M. & Fierke, C. A. (2005). Zinc hydrolases: the mechanisms of zinc-dependent deacetylases. Archives of Biochemistry and Biophysics 433, 71–84.Google Scholar
Hickman, A. B., Perez, Z. N., Zhou, L., Musingarimi, P., Ghirlando, R., Hinshaw, J. E., Craig, N. L. & Dyda, F. (2005). Molecular architecture of a eukaryotic DNA transposase. Nature Structural and Molecular Biology 12, 715–721.Google Scholar
Hickman, A. B., Ronning, D. R., Kotin, R. M. & Dyda, F. (2002). Structural unity among viral origin binding proteins: crystal structure of the nuclease domain of adeno-associated virus Rep. Molecular Cell 10, 327–337.Google Scholar
Hickman, A. B., Ronning, D. R., Perez, Z. N., Kotin, R. M. & Dyda, F. (2004). The nuclease domain of adeno-associated virus rep coordinates replication initiation using two distinct DNA recognition interfaces. Molecular Cell 13, 403–414.Google Scholar
Hickman, A. B., Waninger, S., Scocca, J. J. & Dyda, F. (1997). Molecular organization in site-specific recombination: the catalytic domain of bacteriophage HP1 integrase at 2·7 A resolution. Cell 89, 227–237.Google Scholar
Hoard, D. E. & Goad, W. (1968). Products in the initial stages of digestion of polydeoxynucleotides by pancreatic deoxyribonuclease (DNase I). Journal of Molecular Biology 31, 595–606.Google Scholar
Hopfner, K. P., Karcher, A., Craig, L., Woo, T. T., Carney, J. P. & Tainer, J. A. (2001). Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105, 473–485.Google Scholar
Horton, N. C. (2008). DNA Nucleases. In Protein–Nucleic Acid Interactions (eds. Rice, P. A. & Correll, C. C.), pp. 333–363. Cambridge: Royal Society of Chemistry Publishing.Google Scholar
Horton, N. C. & Perona, J. J. (2004). DNA cleavage by EcoRV endonuclease: two metal ions in three metal ion binding sites. Biochemistry 43, 6841–6857.Google Scholar
Hough, E., Hansen, L. K., Birknes, B., Jynge, K., Hansen, S., Hordvik, A., Little, C., Dodson, E. & Derewenda, Z. (1989). High-resolution (1·5 A) crystal structure of phospholipase C from Bacillus cereus. Nature 338, 357–360.Google Scholar
Houseley, J., Lacava, J. & Tollervey, D. (2006). RNA-quality control by the exosome. Nature Reviews Molecular Cell Biology 7, 529–539.Google Scholar
Hsia, K. C., Li, C. L. & Yuan, H. S. (2005). Structural and functional insight into sugar-nonspecific nucleases in host defense. Current Opinion in Structural Biology 15, 126–134.Google Scholar
Hsiao, Y. Y., Nakagawa, A., Shi, Z., Mitani, S., Xue, D. & Yuan, H. S. (2009). Crystal structure of CRN-4: implications for domain function in apoptotic DNA degradation. Molecular and Cellular Biology 29, 448–457.Google Scholar
Hwang, K. Y., Baek, K., Kim, H. Y. & Cho, Y. (1998). The crystal structure of flap endonuclease-1 from Methanococcus jannaschii. Nature Structural Biology 5, 707–713.Google Scholar
Ip, S. C., Rass, U., Blanco, M. G., Flynn, H. R., Skehel, J. M. & West, S. C. (2008). Identification of Holliday junction resolvases from humans and yeast. Nature 456, 357–361.Google Scholar
Irie, M. & Ohgi, K. (2001). Ribonuclease T2. Methods in Enzymology 341, 42–55.Google Scholar
Ishii, R., Minagawa, A., Takaku, H., Takagi, M., Nashimoto, M. & Yokoyama, S. (2005). Crystal structure of the tRNA 3′ processing endoribonuclease tRNase Z from Thermotoga maritima. Journal of Biological Chemistry 280, 14138–14144.Google Scholar
Ishikawa, K., Watanabe, M., Kuroita, T., Uchiyama, I., Bujnicki, J. M., Kawakami, B., Tanokura, M. & Kobayashi, I. (2005). Discovery of a novel restriction endonuclease by genome comparison and application of a wheat-germ-based cell-free translation assay: PabI (5′-GTA/C) from the hyperthermophilic archaeon Pyrococcus abyssi. Nucleic Acids Research 33, e112.Google Scholar
Ivanov, I., Tainer, J. A. & Mccammon, J. A. (2007). Unraveling the three-metal-ion catalytic mechanism of the DNA repair enzyme endonuclease IV. Proceedings of the National Academy of Sciences USA 104, 1465–1470.Google Scholar
Iwasaki, H., Takahagi, M., Shiba, T., Nakata, A. & Shinagawa, H. (1991). Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure. EMBO Journal 10, 4381–4389.Google Scholar
Jabri, E., Carr, M. B., Hausinger, R. P. & Karplus, P. A. (1995). The crystal structure of urease from Klebsiella aerogenes. Science 268, 998–1004.Google Scholar
Jakubauskas, A., Giedriene, J., Bujnicki, J. M. & Janulaitis, A. (2007). Identification of a single HNH active site in type IIS restriction endonuclease Eco31I. Journal of Molecular Biology 370, 157–169.Google Scholar
James, R., Kleanthous, C. & Moore, G. R. (1996). The biology of E colicins: paradigms and paradoxes. Microbiology 142, 1569–1580.Google Scholar
Jenny, A., Minvielle-Sebastia, L., Preker, P. J. & Keller, W. (1996). Sequence similarity between the 73-kilodalton protein of mammalian CPSF and a subunit of yeast polyadenylation factor I. Science 274, 1514–1517.Google Scholar
Jensch, F. & Kemper, B. (1986). Endonuclease VII resolves Y-junctions in branched DNA in vitro. EMBO Journal 5, 181–189.Google Scholar
Ji, X. (2008). The mechanism of RNase III action: how dicer dices. Current Topics in Microbiology and Immunology 320, 99–116.Google Scholar
Jin, Y., Binkowski, G., Simon, L. D. & Norris, D. (1997). Ho endonuclease cleaves MAT DNA in vitro by an inefficient stoichiometric reaction mechanism. Journal of Biological Chemistry 272, 7352–7359.Google Scholar
Johnson, E. R. & Mckay, D. B. (1999). Mapping the role of active site residues for transducing an ATP-induced conformational change in the bovine 70-kDa heat shock cognate protein. Biochemistry 38, 10823–10830.Google Scholar
Jones, S. J., Worrall, A. F. & Connolly, B. A. (1996). Site-directed mutagenesis of the catalytic residues of bovine pancreatic deoxyribonuclease I. Journal of Molecular Biology 264, 1154–1163.Google Scholar
Jonstrup, A. T., Andersen, K. R., Van, L. B. & Brodersen, D. E. (2007). The 1·4-A crystal structure of the S. pombe Pop2p deadenylase subunit unveils the configuration of an active enzyme. Nucleic Acids Research 35, 3153–3164.Google Scholar
Joshua-Tor, L. (2006). The Argonautes. Cold Spring Harbor Symposia on Quantitative Biology 71, 67–72.Google Scholar
Kadyrov, F. A., Dzantiev, L., Constantin, N. & Modrich, P. (2006). Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126, 297–308.Google Scholar
Kadyrov, F. A., Holmes, S. F., Arana, M. E., Lukianova, O. A., O'Donnell, M., Kunkel, T. A. & Modrich, P. (2007). Saccharomyces cerevisiae MutLalpha is a mismatch repair endonuclease. Journal of Biological Chemistry 282, 37181–37190.Google Scholar
Kaminska, K. H., Kawai, M., Boniecki, M., Kobayashi, I. & Bujnicki, J. M. (2008). Type II restriction endonuclease R.Hpy188I belongs to the GIY-YIG nuclease superfamily, but exhibits an unusual active site. BMC Structural Biology 8, 48.Google Scholar
Kao, H. I. & Bambara, R. A. (2003). The protein components and mechanism of eukaryotic Okazaki fragment maturation. Critical Reviews in Biochemistry and Molecular Biology 38, 433–452.Google Scholar
Karakas, E., Truglio, J. J., Croteau, D., Rhau, B., Wang, L., Van Houten, B. & Kisker, C. (2007). Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad. EMBO Journal 26, 613–622.Google Scholar
Kartha, G., Bello, J. & Harker, D. (1967). Tertiary structure of ribonuclease. Nature 213, 862–865.Google Scholar
Kawano, S., Kakuta, Y., Nakashima, T. & Kimura, M. (2006). Crystal structures of the Nicotiana glutinosa ribonuclease NT in complex with nucleoside monophosphates. Journal of Biochemistry 140, 375–381.Google Scholar
Keck, J. L., Roche, D. D., Lynch, A. S. & Berger, J. M. (2000). Structure of the RNA polymerase domain of E. coli primase. Science 287, 2482–2486.Google Scholar
Keeney, S. (2001). Mechanism and control of meiotic recombination initiation. Current Topics in Developmental Biology 52, 1–53.Google Scholar
Kennedy, A. K., Haniford, D. B. & Mizuuchi, K. (2000). Single active site catalysis of the successive phosphoryl transfer steps by DNA transposases: insights from phosphorothioate stereoselectivity. Cell 101, 295–305.Google Scholar
Khan, S. A. (2005). Plasmid rolling-circle replication: highlights of two decades of research. Plasmid 53, 126–136.Google Scholar
Kim, D. H. & Mobashery, S. (2001). Mechanism-based inhibition of zinc proteases. Current Medicinal Chemistry 8, 959–965.Google Scholar
Kim, D. R., Dai, Y., Mundy, C. L., Yang, W. & Oettinger, M. A. (1999). Mutations of acidic residues in RAG1 define the active site of the V(D)J recombinase. Genes and Development 13, 3070–3080.Google Scholar
Kim, E. E. & Wyckoff, H. W. (1991). Reaction mechanism of alkaline phosphatase based on crystal structures. Two-metal ion catalysis. Journal of Molecular Biology 218, 449–464.Google Scholar
Kim, J. H., Kim, H. D., Ryu, G. H., Kim, D. H., Hurwitz, J. & Seo, Y. S. (2006). Isolation of human Dna2 endonuclease and characterization of its enzymatic properties. Nucleic Acids Research 34, 1854–1864.Google Scholar
Kim, Y., Eom, S. H., Wang, J., Lee, D. S., Suh, S. W. & Steitz, T. A. (1995). Crystal structure of Thermus aquaticus DNA polymerase. Nature 376, 612–616.Google Scholar
Kirsebom, L. A. (2007). RNase P RNA mediated cleavage: substrate recognition and catalysis. Biochimie 89, 1183–1194.Google Scholar
Kleanthous, C., Kuhlmann, U. C., Pommer, A. J., Ferguson, N., Radford, S. E., Moore, G. R., James, R. & Hemmings, A. M. (1999). Structural and mechanistic basis of immunity toward endonuclease colicins. Nature Structural Biology 6, 243–252.Google Scholar
Klein, D. J. & Ferre-D'amare, A. R. (2006). Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313, 1752–1756.Google Scholar
Klett, R. P., Cerami, A. & Reich, E. (1968). Exonuclease VI, a new nuclease activity associated with E. coli DNA polymerase. Proceedings of the National Academy of Sciences USA 60, 943–950.Google Scholar
Ko, T. P., Liao, C. C., Ku, W. Y., Chak, K. F. & Yuan, H. S. (1999). The crystal structure of the DNase domain of colicin E7 in complex with its inhibitor Im7 protein. Structure 7, 91–102.Google Scholar
Kobe, B. & Deisenhofer, J. (1996). Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. Journal of Molecular Biology 264, 1028–1043.Google Scholar
Kolade, O. O., Carr, S. B., Kuhlmann, U. C., Pommer, A., Kleanthous, C., Bouchcinsky, C. A. & Hemmings, A. M. (2002). Structural aspects of the inhibition of DNase and rRNase colicins by their immunity proteins. Biochimie 84, 439–446.Google Scholar
Kolodner, R., Hall, S. D. & Luisi-Deluca, C. (1994). Homologous pairing proteins encoded by the Escherichia coli recE and recT genes. Molecular Microbiology 11, 23–30.Google Scholar
Koonin, E. V. & Ilyina, T. V. (1993). Computer-assisted dissection of rolling circle DNA replication. Biosystems 30, 241–268.Google Scholar
Kosinski, J., Plotz, G., Guarne, A., Bujnicki, J. M. & Friedhoff, P. (2008). The PMS2 subunit of human MutLalpha contains a metal ion binding domain of the iron-dependent repressor protein family. Journal of Molecular Biology 382, 610–627.Google Scholar
Kostelecky, B., Pohl, E., Vogel, A., Schilling, O. & Meyer-Klaucke, W. (2006). The crystal structure of the zinc phosphodiesterase from Escherichia coli provides insight into function and cooperativity of tRNase Z-family proteins. Journal of Bacteriology 188, 1607–1614.Google Scholar
Kovall, R. & Matthews, B. W. (1997). Toroidal structure of lambda-exonuclease. Science 277, 1824–1827.Google Scholar
Kowalczykowski, S. C., Dixon, D. A., Eggleston, A. K., Lauder, S. D. & Rehrauer, W. M. (1994). Biochemistry of homologous recombination in Escherichia coli. Microbiology Reviews 58, 401–465.Google Scholar
Kruger, K., Grabowski, P. J., Zaug, A. J., Sands, J., Gottschling, D. E. & Cech, T. R. (1982). Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31, 147–157.Google Scholar
Kuhlmann, U. C., Moore, G. R., James, R., Kleanthous, C. & Hemmings, A. M. (1999). Structural parsimony in endonuclease active sites: should the number of homing endonuclease families be redefined? FEBS Letters 463, 1–2.Google Scholar
Kunitz, M. (1950). Crystalline desoxyribonuclease; isolation and general properties; spectrophotometric method for the measurement of desoxyribonuclease activity. Journal of General Physiology 33, 349–362.Google Scholar
Kwon, H. J., Tirumalai, R., Landy, A. & Ellenberger, T. (1997). Flexibility in DNA recombination: structure of the lambda integrase catalytic core. Science 276, 126–131.Google Scholar
Lagerback, P., Andersson, E., Malmberg, C. & Carlson, K. (2009). Bacteriophage T4 endonuclease II, a promiscuous GIY-YIG nuclease, binds as a tetramer to two DNA substrates. Nucleic Acids Research 37, 6174–6183.Google Scholar
Lagunavicius, A., Sasnauskas, G., Halford, S. E. & Siksnys, V. (2003). The metal-independent type IIs restriction enzyme BfiI is a dimer that binds two DNA sites but has only one catalytic centre. Journal of Molecular Biology 326, 1051–1064.Google Scholar
Lam, A. F., Krogh, B. O. & Symington, L. S. (2008). Unique and overlapping functions of the Exo1, Mre11 and Pso2 nucleases in DNA repair. DNA Repair (Amsterdam)7, 655–662.Google Scholar
Landree, M. A., Wibbenmeyer, J. A. & Roth, D. B. (1999). Mutational analysis of RAG1 and RAG2 identifies three catalytic amino acids in RAG1 critical for both cleavage steps of V(D)J recombination. Genes and Development 13, 3059–3069.Google Scholar
Laneve, P., Altieri, F., Fiori, M. E., Scaloni, A., Bozzoni, I. & Caffarelli, E. (2003). Purification, cloning, and characterization of XendoU, a novel endoribonuclease involved in processing of intron-encoded small nucleolar RNAs in Xenopus laevis. Journal of Biological Chemistry 278, 13026–13032.Google Scholar
Laneve, P., Gioia, U., Ragno, R., Altieri, F., Di Franco, C., Santini, T., Arceci, M., Bozzoni, I. & Caffarelli, E. (2008). The tumor marker human placental protein 11 is an endoribonuclease. Journal of Biological Chemistry 283, 34712–34719.Google Scholar
Lange, S. J. & Que, L. JR. ( 1998). Oxygen activating nonheme iron enzymes. Current Opinion in Chemical Biology 2, 159–172.Google Scholar
Lapkouski, M., Panjikar, S., Janscak, P., Smatanova, I. K., Carey, J., Ettrich, R. & Csefalvay, E. (2009). Structure of the motor subunit of type I restriction–modification complex EcoR124I. Nature Structural and Molecular Biology 16, 94–95.Google Scholar
Larkin, C., Datta, S., Harley, M. J., Anderson, B. J., Ebie, A., Hargreaves, V. & Schildbach, J. F. (2005). Inter- and intramolecular determinants of the specificity of single-stranded DNA binding and cleavage by the F factor relaxase. Structure 13, 1533–1544.Google Scholar
Larkin, C., Haft, R. J., Harley, M. J., Traxler, B. & Schildbach, J. F. (2007). Roles of active site residues and the HUH motif of the F plasmid TraI relaxase. Journal of Biological Chemistry 282, 33707–33713.Google Scholar
Laskowski, M. SR. (1985). Nucleases: historical respectives. In Nucleases (eds. Linn, S. M. & Roberts, R. J.), pp. 1–21. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Lee, B. I., Kim, K. H., Park, S. J., Eom, S. H., Song, H. K. & Suh, S. W. (2004). Ring-shaped architecture of RecR: implications for its role in homologous recombinational DNA repair. EMBO Journal 23, 2029–2038.Google Scholar
Lee, B. I. & Wilson, D. M. 3RD. (1999). The RAD2 domain of human exonuclease 1 exhibits 5′ to 3′ exonuclease and flap structure-specific endonuclease activities. Journal of Biological Chemistry 274, 37763–37769.Google Scholar
Lee, F. S., Auld, D. S. & Vallee, B. L. (1989). Tryptophan fluorescence as a probe of placental ribonuclease inhibitor binding to angiogenin. Biochemistry 28, 219–224.Google Scholar
Lee, J. Y., Chang, J., Joseph, N., Ghirlando, R., Rao, D. N. & Yang, W. (2005). MutH complexed with Hemi- and unmethylated DNAs: coupling base recognition and DNA cleavage. Molecular Cell 20, 155–166.Google Scholar
Lee, K. P., Dey, M., Neculai, D., Cao, C., Dever, T. E. & Sicheri, F. (2008). Structure of the dual enzyme Ire1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 132, 89–100.Google Scholar
Lehman, I. R. & Nussbaum, A. L. (1964). The deoxyribonucleases of Escherichia coli V on the specificity of exonuclease I (phosphodiesterase). Journal of Biological Chemistry 239, 2628–2636.Google Scholar
Li, G. M. (2008). Mechanisms and functions of DNA mismatch repair. Cell Research 18, 85–98.Google Scholar
Li, W., Kamtekar, S., Xiong, Y., Sarkis, G. J., Grindley, N. D. & Steitz, T. A. (2005). Structure of a synaptic gammadelta resolvase tetramer covalently linked to two cleaved DNAs. Science 309, 1210–1215.Google Scholar
Lilley, D. M. (2005). Structure, folding and mechanisms of ribozymes. Current Opinion in Structural Biology 15, 313–323.Google Scholar
Lilley, D. M. & White, M. F. (2001). The junction-resolving enzymes. Nature Reviews Molecular Cell Biology 2, 433–443.Google Scholar
Liu, Q., Greimann, J. C. & Lima, C. D. (2006). Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223–1237.Google Scholar
Liu, X., Zou, H., Slaughter, C. & Wang, X. (1997). DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175–184.Google Scholar
Liu, Y., Kao, H. I. & Bambara, R. A. (2004). Flap endonuclease 1: a central component of DNA metabolism. Annual Review of Biochemistry 73, 589–615.Google Scholar
Llosa, M., Gomis-Ruth, F. X., Coll, M. & De La Cruz Fd, F. (2002). Bacterial conjugation: a two-step mechanism for DNA transport. Molecular Microbiology 45, 1–8.Google Scholar
Loll, P. J., Quirk, S., Lattman, E. E. & Garavito, R. M. (1995). X-ray crystal structures of staphylococcal nuclease complexed with the competitive inhibitor cobalt(II) and nucleotide. Biochemistry 34, 4316–4324.Google Scholar
Lorentzen, E., Basquin, J., Tomecki, R., Dziembowski, A. & Conti, E. (2008). Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Molecular Cell 29, 717–728.Google Scholar
Lorentzen, E., Dziembowski, A., Lindner, D., Seraphin, B. & Conti, E. (2007). RNA channelling by the archaeal exosome. EMBO Reports 8, 470–476.Google Scholar
Lorentzen, E., Walter, P., Fribourg, S., Evguenieva-Hackenberg, E., Klug, G. & Conti, E. (2005). The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nature Structural and Molecular Biology 12, 575–581.Google Scholar
Lyamichev, V., Brow, M. A. & Dahlberg, J. E. (1993). Structure-specific endonucleolytic cleavage of nucleic acids by eubacterial DNA polymerases. Science 260, 778–783.Google Scholar
Lykke-Andersen, S., Brodersen, D. E. & Jensen, T. H. (2009). Origins and activities of the eukaryotic exosome. Journal of Cell Science 122, 1487–1494.Google Scholar
Lyons, T. J. & Eide, D. J. (2006). Transport and storage of metal ions in biology. In Biological Inorganic Chemistry: Structure and Reactivity (eds. Bertini, I., Gray, H. B., Stiefel, E. I. & Valentine, J. S.), pp. 57–77. Herndon, VA: University Science Books.Google Scholar
Macelrevey, C., Salter, J. D., Krucinska, J. & Wedekind, J. E. (2008). Structural effects of nucleobase variations at key active site residue Ade38 in the hairpin ribozyme. RNA 14, 1600–1616.Google Scholar
Macmaster, R., Sedelnikova, S., Baker, P. J., Bolt, E. L., Lloyd, R. G. & Rafferty, J. B. (2006). RusA Holliday junction resolvase: DNA complex structure – insights into selectivity and specificity. Nucleic Acids Research 34, 5577–5584.Google Scholar
Macrae, I. J. & Doudna, J. A. (2007). Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Current Opinion in Structural Biology 17, 138–145.Google Scholar
Macrae, I. J., Zhou, K. & Doudna, J. A. (2007). Structural determinants of RNA recognition and cleavage by Dicer. Nature Structural and Molecular Biology 14, 934–940.Google Scholar
Macrae, I. J., Zhou, K., Li, F., Repic, A., Brooks, A. N., Cande, W. Z., Adams, P. D. & Doudna, J. A. (2006). Structural basis for double-stranded RNA processing by Dicer. Science 311, 195–198.CrossRefGoogle Scholar
Maguire, M. E. & Cowan, J. A. (2002). Magnesium chemistry and biochemistry. Biometals 15, 203–210.Google Scholar
Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I. & Koonin, E. V. (2006). A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biology Direct 1, 7.Google Scholar
Mandel, C. R., Kaneko, S., Zhang, H., Gebauer, D., Vethantham, V., Manley, J. L. & Tong, L. (2006). Polyadenylation factor CPSF-73 is the pre-mRNA 3′-end-processing endonuclease. Nature 444, 953–956.Google Scholar
Marti, T. M. & Fleck, O. (2004). DNA repair nucleases. Cellular and Molecular Life Science 61, 336–354.Google Scholar
Martinez Valle, F., Balada, E., Ordi-Ros, J. & Vilardell-Tarres, M. (2008). DNase 1 and systemic lupus erythematosus. Autoimmunity Reviews 7, 359–363.Google Scholar
Marzluff, W. F., Wagner, E. J. & Duronio, R. J. (2008). Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nature Reviews Genetics 9, 843–854.Google Scholar
Masuda-Sasa, T., Imamura, O. & Campbell, J. L. (2006). Biochemical analysis of human Dna2. Nucleic Acids Research 34, 1865–1875.Google Scholar
Mate, M. J. & Kleanthous, C. (2004). Structure-based analysis of the metal-dependent mechanism of H-N-H endonucleases. Journal of Biological Chemistry 279, 34763–34769.Google Scholar
Mathy, N., Benard, L., Pellegrini, O., Daou, R., Wen, T. & Condon, C. (2007). 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129, 681–692.Google Scholar
Mazzarella, L., Capasso, S., Demasi, D., Di Lorenzo, G., Mattia, C. A. & Zagari, A. (1993). Bovine seminal ribonuclease: structure at 1·9 A resolution. Acta Crystallographica D: Biological Crystallography 49, 389–402.Google Scholar
Mchenry, C. S. (1985). DNA polymerase III holoenzyme of Escherichia coli: components and function of a true replicative complex. Molecular and Cellular Biochemistry 66, 71–85.Google Scholar
Merlino, A., Ercole, C., Picone, D., Pizzo, E., Mazzarella, L. & Sica, F. (2008). The buried diversity of bovine seminal ribonuclease: shape and cytotoxicity of the swapped non-covalent form of the enzyme. Journal of Molecular Biology 376, 427–437.Google Scholar
Michel, F., Costa, M. & Westhof, E. (2009). The ribozyme core of group II introns: a structure in want of partners. Trends in Biochemical Sciences 34, 189–199.Google Scholar
Midtgaard, S. F., Assenholt, J., Jonstrup, A. T., Van, L. B., Jensen, T. H. & Brodersen, D. E. (2006). Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proceedings of the National Academy of Sciences USA 103, 11898–11903.Google Scholar
Mildvan, A. S., Xia, Z., Azurmendi, H. F., Saraswat, V., Legler, P. M., Massiah, M. A., Gabelli, S. B., Bianchet, M. A., Kang, L. W. & Amzel, L. M. (2005). Structures and mechanisms of Nudix hydrolases. Archives of Biochemistry and Biophysics 433, 129–143.Google Scholar
Mimitou, E. P. & Symington, L. S. (2009). DNA end resection: many nucleases make light work. DNA Repair (Amsterdam) 8, 983–995.Google Scholar
Minagawa, A., Takaku, H., Takagi, M. & Nashimoto, M. (2004). A novel endonucleolytic mechanism to generate the CCA 3′ termini of tRNA molecules in Thermotoga maritima. Journal of Biological Chemistry 279, 15688–15697.Google Scholar
Miyazono, K., Watanabe, M., Kosinski, J., Ishikawa, K., Kamo, M., Sawasaki, T., Nagata, K., Bujnicki, J. M., Endo, Y., Tanokura, M. & Kobayashi, I. (2007). Novel protein fold discovered in the PabI family of restriction enzymes. Nucleic Acids Research 35, 1908–1918.Google Scholar
Mol, C. D., Izumi, T., Mitra, S. & Tainer, J. A. (2000). DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected]. Nature 403, 451–456.Google Scholar
Mol, C. D., Kuo, C. F., Thayer, M. M., Cunningham, R. P. & Tainer, J. A. (1995). Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374, 381–386.Google Scholar
Monzingo, A. F., Ozburn, A., Xia, S., Meyer, R. J. & Robertus, J. D. (2007). The structure of the minimal relaxase domain of MobA at 2·1 A resolution. Journal of Molecular Biology 366, 165–178.Google Scholar
Moore, M. J. & Proudfoot, N. J. (2009). Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688–700.Google Scholar
Morita, M., Stamp, G., Robins, P., Dulic, A., Rosewell, I., Hrivnak, G., Daly, G., Lindahl, T. & Barnes, D. E. (2004). Gene-targeted mice lacking the Trex1 (DNase III) 3′→5′ DNA exonuclease develop inflammatory myocarditis. Molecular and Cellular Biology 24, 6719–6727.Google Scholar
Moshous, D., Callebaut, I., De Chasseval, R., Corneo, B., Cavazzana-Calvo, M., Le Deist, F., Tezcan, I., Sanal, O., Bertrand, Y., Philippe, N., Fischer, A. & De Villartay, J. P. (2001). Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 105, 177–186.Google Scholar
Moure, C. M., Gimble, F. S. & Quiocho, F. A. (2008). Crystal structures of I-SceI complexed to nicked DNA substrates: snapshots of intermediates along the DNA cleavage reaction pathway. Nucleic Acids Research 36, 3287–3296.Google Scholar
Muftuoglu, M., Oshima, J., Von Kobbe, C., Cheng, W. H., Leistritz, D. F. & Bohr, V. A. (2008). The clinical characteristics of Werner syndrome: molecular and biochemical diagnosis. Human Genetics 124, 369–377.Google Scholar
Muro-Pastor, A. M., Flores, E., Herrero, A. & Wolk, C. P. (1992). Identification, genetic analysis and characterization of a sugar-non-specific nuclease from the cyanobacterium Anabaena sp. PCC 7120. Molecular Microbiology 6, 3021–3030.Google Scholar
Murray, N. E. (2000). Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiology and Molecular Biology Reviews 64, 412–434.Google Scholar
Muyrers, J. P., Zhang, Y. & Stewart, A. F. (2000). ET-cloning: think recombination first. Genetic Engineering (New York) 22, 77–98.Google Scholar
Nagata, S. (2007). Autoimmune diseases caused by defects in clearing dead cells and nuclei expelled from erythroid precursors. Immunological Reviews 220, 237–250.Google Scholar
Nandakumar, J., Schwer, B., Schaffrath, R. & Shuman, S. (2008). RNA repair: an antidote to cytotoxic eukaryal RNA damage. Molecular Cell 31, 278–286.Google Scholar
Newman, M., Lunnen, K., Wilson, G., Greci, J., Schildkraut, I. & Phillips, S. E. (1998). Crystal structure of restriction endonuclease BglI bound to its interrupted DNA recognition sequence. EMBO Journal 17, 5466–5476.Google Scholar
Newman, M., Murray-Rust, J., Lally, J., Rudolf, J., Fadden, A., Knowles, P. P., White, M. F. & Mcdonald, N. Q. (2005). Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO Journal 24, 895–905.Google Scholar
Nichols, M. D., Deangelis, K., Keck, J. L. & Berger, J. M. (1999). Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO Journal 18, 6177–6188.Google Scholar
Niiranen, L., Altermark, B., Brandsdal, B. O., Leiros, H. K., Helland, R., Smalas, A. O. & Willassen, N. P. (2008). Effects of salt on the kinetics and thermodynamic stability of endonuclease I from Vibrio salmonicida and Vibrio cholerae. FEBS Journal 275, 1593–1605.Google Scholar
Nishino, T., Komori, K., Ishino, Y. & Morikawa, K. (2003). X-ray and biochemical anatomy of an archaeal XPF/Rad1/Mus81 family nuclease: similarity between its endonuclease domain and restriction enzymes. Structure 11, 445–457.Google Scholar
Niv, M. Y., Ripoll, D. R., Vila, J. A., Liwo, A., Vanamee, E. S., Aggarwal, A. K., Weinstein, H. & Scheraga, H. A. (2007). Topology of Type II REases revisited; structural classes and the common conserved core. Nucleic Acids Research 35, 2227–2237.Google Scholar
Nowotny, M. (2009). Retroviral integrase superfamily: the structural perspective. EMBO Reports 10, 144–151.Google Scholar
Nowotny, M., Cerritelli, S. M., Ghirlando, R., Gaidamakov, S. A., Crouch, R. J. & Yang, W. (2008). Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. EMBO Journal 27, 1172–1181.Google Scholar
Nowotny, M., Gaidamakov, S. A., Crouch, R. J. & Yang, W. (2005). Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121, 1005–1016.Google Scholar
Nowotny, M., Gaidamakov, S. A., Ghirlando, R., Cerritelli, S. M., Crouch, R. J. & Yang, W. (2007). Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Molecular Cell 28, 264–276.Google Scholar
Nowotny, M. & Yang, W. (2006). Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO Journal 25, 1924–1933.Google Scholar
Nowotny, M. & Yang, W. (2009). Structural and functional modules in RNA interference. Current Opinion in Structural Biology 19, 286–293.Google Scholar
O'DONOVAN, A., Davies, A. A., Moggs, J. G., West, S. C. & Wood, R. D. (1994). XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature 371, 432–435.Google Scholar
Obmolova, G., Ban, C., Hsieh, P. & Yang, W. (2000). Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407, 703–710.Google Scholar
Ollis, D. L., Brick, P., Hamlin, R., Xuong, N. G. & Steitz, T. A. (1985). Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313, 762–766.Google Scholar
Olmo, N., Turnay, J., Gonzalez De Buitrago, G., Lopez De Silanes, I., Gavilanes, J. G. & Lizarbe, M. A. (2001). Cytotoxic mechanism of the ribotoxin alpha-sarcin. Induction of cell death via apoptosis. European Journal of Biochemistry 268, 2113–2123.Google Scholar
Orlowski, J. & Bujnicki, J. M. (2008). Structural and evolutionary classification of type II restriction enzymes based on theoretical and experimental analyses. Nucleic Acids Research 36, 3552–3569.Google Scholar
Pan, C. Q. & Lazarus, R. A. (1999). Ca2+-dependent activity of human DNase I and its hyperactive variants. Protein Science 8, 1780–1788.Google Scholar
Paquin, B., O'KELLY, C. J. & Lang, B. F. (1995). Intron-encoded open reading frame of the GIY-YIG subclass in a plastid gene. Current Genetics 28, 97–99.Google Scholar
Parker, R. & Song, H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nature Structural and Molecular Biology 11, 121–127.Google Scholar
Parrish, J. Z. & Xue, D. (2006). Cuts can kill: the roles of apoptotic nucleases in cell death and animal development. Chromosoma 115, 89–97.Google Scholar
Patel, A. A. & Steitz, J. A. (2003). Splicing double: insights from the second spliceosome. Nature Reviews Molecular Cell Biology 4, 960–970.Google Scholar
Pauling, L. (1961). The Nature of the Chemical Bond. Ithaca: Cornell University Press.Google Scholar
Paull, T. T. & Gellert, M. (1998). The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Molecular Cell 1, 969–979.Google Scholar
Paull, T. T. & Gellert, M. (1999). Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes and Development 13, 1276–1288.Google Scholar
Peebles, C. L., Perlman, P. S., Mecklenburg, K. L., Petrillo, M. L., Tabor, J. H., Jarrell, K. A. & Cheng, H. L. (1986). A self-splicing RNA excises an intron lariat. Cell 44, 213–223.Google Scholar
Pena, V., Rozov, A., Fabrizio, P., Luhrmann, R. & Wahl, M. C. (2008). Structure and function of an RNase H domain at the heart of the spliceosome. EMBO Journal 27, 2929–2940.Google Scholar
Perrino, F. W., Harvey, S., Mcmillin, S. & Hollis, T. (2005). The human TREX2 3′→5′-exonuclease structure suggests a mechanism for efficient nonprocessive DNA catalysis. Journal of Biological Chemistry 280, 15212–15218.Google Scholar
Perry, J. J., Yannone, S. M., Holden, L. G., Hitomi, C., Asaithamby, A., Han, S., Cooper, P. K., Chen, D. J. & Tainer, J. A. (2006a). WRN exonuclease structure and molecular mechanism imply an editing role in DNA end processing. Nature Structural and Molecular Biology 13, 414–422.Google Scholar
Perry, K., Hwang, Y., Bushman, F. D. & Van Duyne, G. D. (2006b). Structural basis for specificity in the poxvirus topoisomerase. Molecular Cell 23, 343–354.Google Scholar
Pidcock, E. & Moore, G. R. (2001). Structural characteristics of protein binding sites for calcium and lanthanide ions. Journal of Biology and Inorganic Chemistry 6, 479–489.Google Scholar
Pingoud, A., Fuxreiter, M., Pingoud, V. & Wende, W. (2005). Type II restriction endonucleases: structure and mechanism. Cellular and Molecular Life Science 62, 685–707.Google Scholar
Pingoud, V., Wende, W., Friedhoff, P., Reuter, M., Alves, J., Jeltsch, A., Mones, L., Fuxreiter, M. & Pingoud, A. (2009). On the divalent metal ion dependence of DNA cleavage by restriction endonucleases of the EcoRI family. Journal of Molecular Biology 393, 140–160.Google Scholar
Pontius, B. W., Lott, W. B. & Von Hippel, P. H. (1997). Observations on catalysis by hammerhead ribozymes are consistent with a two-divalent-metal-ion mechanism. Proceedings of the National Academy of Sciences USA 94, 2290–2294.Google Scholar
Pouliot, J. J., Yao, K. C., Robertson, C. A. & Nash, H. A. (1999). Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286, 552–555.Google Scholar
Rafferty, J. B., Bolt, E. L., Muranova, T. A., Sedelnikova, S. E., Leonard, P., Pasquo, A., Baker, P. J., Rice, D. W., Sharples, G. J. & Lloyd, R. G. (2003). The structure of Escherichia coli RusA endonuclease reveals a new Holliday junction DNA binding fold. Structure 11, 1557–1567.Google Scholar
Raines, R. T. (1998). Ribonuclease A. Chem Rev 98, 1045–1066.Google Scholar
Rangarajan, E. S. & Shankar, V. (2001). Sugar non-specific endonucleases. FEMS Microbiology Reviews 25, 583–613.Google Scholar
Redinbo, M. R., Champoux, J. J. & Hol, W. G. (2000). Novel insights into catalytic mechanism from a crystal structure of human topoisomerase I in complex with DNA. Biochemistry 39, 6832–6840.Google Scholar
Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J. & Hol, W. G. (1998). Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504–1513.Google Scholar
Reed, R. R. (1981). Transposon-mediated site-specific recombination: a defined in vitro system. Cell 25, 713–719.Google Scholar
Reha-Krantz, L. J. (2010). DNA polymerase proofreading: multiple roles maintain genome stability. Biochimica et Biophysica Acta 1804, 1049–1063.Google Scholar
Reiter, T. A., Reiter, N. J. & Rusnak, F. (2002). Mn2+ is a native metal ion activator for bacteriophage lambda protein phosphatase. Biochemistry 41, 15404–15409.Google Scholar
Renzi, F., Caffarelli, E., Laneve, P., Bozzoni, I., Brunori, M. & Vallone, B. (2006). The structure of the endoribonuclease XendoU: From small nucleolar RNA processing to severe acute respiratory syndrome coronavirus replication. Proceedings of the National Academy of Sciences USA 103, 12365–12370.Google Scholar
Rice, P. & Mizuuchi, K. (1995). Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell 82, 209–220.Google Scholar
Richardson, J. M., Colloms, S. D., Finnegan, D. J. & Walkinshaw, M. D. (2009). Molecular architecture of the Mos1 paired-end complex: the structural basis of DNA transposition in a eukaryote. Cell 138, 1096–1108.Google Scholar
Ritchie, D. B., Schellenberg, M. J., Gesner, E. M., Raithatha, S. A., Stuart, D. T. & Macmillan, A. M. (2008). Structural elucidation of a PRP8 core domain from the heart of the spliceosome. Nature Structural and Molecular Biology 15, 1199–1205.Google Scholar
Roberts, R. J., Vincze, T., Posfai, J. & Macelis, D. (2009). REBASE – a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Research 38 (Database Issue), D234–236.Google Scholar
Romani, A. & Scarpa, A. (1992). Regulation of cell magnesium. Archives of Biochemistry and Biophysics 298, 1–12.Google Scholar
Romier, C., Dominguez, R., Lahm, A., Dahl, O. & Suck, D. (1998). Recognition of single-stranded DNA by nuclease P1: high resolution crystal structures of complexes with substrate analogs. Proteins 32, 414–424.Google Scholar
Rupert, P. B., Massey, A. P., Sigurdsson, S. T. & Ferre-D'amare, A. R. (2002). Transition state stabilization by a catalytic RNA. Science 298, 1421–1424.Google Scholar
Rutkoski, T. J. & Raines, R. T. (2008). Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity. Current Pharmaceutical Biotechnology 9, 185–189.Google Scholar
Ryan, K., Calvo, O. & Manley, J. L. (2004). Evidence that polyadenylation factor CPSF-73 is the mRNA 3′ processing endonuclease. RNA 10, 565–573.Google Scholar
Saenger, W. (1984). Principles of Nucleic Acid Structure, New York, NY: Springer.Google Scholar
Salvo, J. J. & Grindley, N. D. (1988). The gamma delta resolvase bends the res site into a recombinogenic complex. EMBO Journal 7, 3609–3616.Google Scholar
Sam, M. D. & Perona, J. J. (1999). Catalytic roles of divalent metal ions in phosphoryl transfer by EcoRV endonuclease. Biochemistry 38, 6576–6586.Google Scholar
Sasnauskas, G., Connolly, B. A., Halford, S. E. & Siksnys, V. (2007). Site-specific DNA transesterification catalyzed by a restriction enzyme. Proceedings of the National Academy of Sciences USA 104, 2115–2120.Google Scholar
Sasnauskas, G., Zakrys, L., Zaremba, M., Cosstick, R., Gaynor, J. W., Halford, S. E. & Siksnys, V. (2010). A novel mechanism for the scission of double-stranded DNA: BfiI cuts both 3′–5′ and 5′–3′ strands by rotating a single active site. Nucleic Acids Research 38, 2399–2410.Google Scholar
Scherly, D., Nouspikel, T., Corlet, J., Ucla, C., Bairoch, A. & Clarkson, S. G. (1993). Complementation of the DNA repair defect in xeroderma pigmentosum group G cells by a human cDNA related to yeast RAD2. Nature 363, 182–185.Google Scholar
Schiffer, S., Rosch, S. & Marchfelder, A. (2002). Assigning a function to a conserved group of proteins: the tRNA 3′-processing enzymes. EMBO Journal 21, 2769–2777.Google Scholar
Schneider, C., Leung, E., Brown, J. & Tollervey, D. (2009). The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Research 37, 1127–1140.Google Scholar
Schoeffler, A. J. & Berger, J. M. (2008). DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Quarterly Review of Biophysics 41, 41–101.Google Scholar
Schulga, A. A., Nurkiyanova, K. M., Zakharyev, V. M., Kirpichnikov, M. P. & Skryabin, K. G. (1992). Cloning of the gene encoding RNase binase from Bacillus intermedius 7P. Nucleic Acids Research 20, 2375.Google Scholar
Schuster, S. C., Miller, W., Ratan, A., Tomsho, L. P., Giardine, B., Kasson, L. R., Harris, R. S., Petersen, D. C., Zhao, F., Qi, J., Alkan, C., Kidd, J. M., Sun, Y., Drautz, D. I., Bouffard, P., Muzny, D. M., Reid, J. G., Nazareth, L. V., Wang, Q., Burhans, R., Riemer, C., Wittekindt, N. E., Moorjani, P., Tindall, E. A., Danko, C. G., Teo, W. S., Buboltz, A. M., Zhang, Z., Ma, Q., Oosthuysen, A., Steenkamp, A. W., Oostuisen, H., Venter, P., Gajewski, J., Zhang, Y., Pugh, B. F., Makova, K. D., Nekrutenko, A., Mardis, E. R., Patterson, N., Pringle, T. H., Chiaromonte, F., Mullikin, J. C., Eichler, E. E., Hardison, R. C., Gibbs, R. A., Harkins, T. T. & Hayes, V. M. (2010). Complete Khoisan and Bantu genomes from southern Africa. Nature 463, 943–947.Google Scholar
Scott, W. G., Murray, J. B., Arnold, J. R., Stoddard, B. L. & Klug, A. (1996). Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science 274, 2065–2069.Google Scholar
Setlow, P. & Kornberg, A. (1972). Deoxyribonucleic acid polymerase: two distinct enzymes in one polypeptide. II. A proteolytic fragment containing the 5′ leads to 3′ exonuclease function. Restoration of intact enzyme functions from the two proteolytic fragments. Journal of Biological Chemistry 247, 232–240.Google Scholar
Sharma, S., Sommers, J. A., Driscoll, H. C., Uzdilla, L., Wilson, T. M. & Brosh, R. M. JR. (2003). The exonucleolytic and endonucleolytic cleavage activities of human exonuclease 1 are stimulated by an interaction with the carboxyl-terminal region of the Werner syndrome protein. Journal of Biological Chemistry 278, 23487–23496.Google Scholar
Sharples, G. J., Chan, S. N., Mahdi, A. A., Whitby, M. C. & Lloyd, R. G. (1994). Processing of intermediates in recombination and DNA repair: identification of a new endonuclease that specifically cleaves Holliday junctions. EMBO Journal 13, 6133–6142.Google Scholar
Shen, B., Singh, P., Liu, R., Qiu, J., Zheng, L., Finger, L. D. & Alas, S. (2005). Multiple but dissectible functions of FEN-1 nucleases in nucleic acid processing, genome stability and diseases. Bioessays 27, 717–729.Google Scholar
Shevelev, I. V., Ramadan, K. & Hubscher, U. (2002). The TREX2 3′→5′ exonuclease physically interacts with DNA polymerase delta and increases its accuracy. ScientificWorld Journal 2, 275–281.Google Scholar
Sidrauski, C. & Walter, P. (1997). The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031–1039.Google Scholar
Silverman, R. H. (2007). Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. Journal of Virology 81, 12720–12729.Google Scholar
Singleton, M. R., Dillingham, M. S., Gaudier, M., Kowalczykowski, S. C. & Wigley, D. B. (2004). Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432, 187–193.Google Scholar
Sinha, K. M., Unciuleac, M. C., Glickman, M. S. & Shuman, S. (2009). AdnAB: a new DSB-resecting motor-nuclease from mycobacteria. Genes and Development 23, 1423–1437.Google Scholar
Sokolowska, M., Czapinska, H. & Bochtler, M. (2009). Crystal structure of the beta beta alpha-Me type II restriction endonuclease Hpy99I with target DNA. Nucleic Acids Research 37, 3799–3810.Google Scholar
Sokolowska, M., Kaus-Drobek, M., Czapinska, H., Tamulaitis, G., Szczepanowski, R. H., Urbanke, C., Siksnys, V. & Bochtler, M. (2007). Monomeric restriction endonuclease BcnI in the apo form and in an asymmetric complex with target DNA. Journal of Molecular Biology 369, 722–734.Google Scholar
Solaro, P. C., Birkenkamp, K., Pfeiffer, P. & Kemper, B. (1993). Endonuclease VII of phage T4 triggers mismatch correction in vitro. Journal of Molecular Biology 230, 868–877.Google Scholar
Sorek, R., Kunin, V. & Hugenholtz, P. (2008). CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nature Reviews Microbiology 6, 181–186.Google Scholar
Spiegel, P. C., Chevalier, B., Sussman, D., Turmel, M., Lemieux, C. & Stoddard, B. L. (2006). The structure of I-CeuI homing endonuclease: Evolving asymmetric DNA recognition from a symmetric protein scaffold. Structure 14, 869–880.Google Scholar
Stahl, M. M., Thomason, L., Poteete, A. R., Tarkowski, T., Kuzminov, A. & Stahl, F. W. (1997). Annealing vs. invasion in phage lambda recombination. Genetics 147, 961–977.Google Scholar
Stahley, M. R. & Strobel, S. A. (2005). Structural evidence for a two-metal-ion mechanism of group I intron splicing. Science 309, 1587–1590.Google Scholar
Stahley, M. R. & Strobel, S. A. (2006). RNA splicing: group I intron crystal structures reveal the basis of splice site selection and metal ion catalysis. Current Opinion in Structural Biology 16, 319–326.Google Scholar
Stec, B., Holtz, K. M. & Kantrowitz, E. R. (2000). A revised mechanism for the alkaline phosphatase reaction involving three metal ions. Journal of Molecular Biology 299, 1303–1311.Google Scholar
Steiniger-White, M., Rayment, I. & Reznikoff, W. S. (2004). Structure/function insights into Tn5 transposition. Current Opinion in Structural Biology 14, 50–57.Google Scholar
Steitz, T. A. (1998). A mechanism for all polymerases. Nature 391, 231–232.Google Scholar
Steitz, T. A. & Steitz, J. A. (1993). A general two-metal-ion mechanism for catalytic RNA. Proceedings of the National Academy of Sciences USA 90, 6498–6502.Google Scholar
Stephenson, J. B. (2008). Aicardi–Goutieres syndrome (AGS). European Journal of Paediatric Neurology 12, 355–358.Google Scholar
Stetson, D. B., Ko, J. S., Heidmann, T. & Medzhitov, R. (2008). Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587–598.Google Scholar
Stoddard, B. L. (2005). Homing endonuclease structure and function. Quarterly Reviews of Biophysics 38, 49–95.Google Scholar
Stuckey, J. A. & Dixon, J. E. (1999). Crystal structure of a phospholipase D family member. Nature Structural Biology 6, 278–284.Google Scholar
Subramanya, H. S., Arciszewska, L. K., Baker, R. A., Bird, L. E., Sherratt, D. J. & Wigley, D. B. (1997). Crystal structure of the site-specific recombinase, XerD. EMBO Journal 16, 5178–5187.Google Scholar
Suck, D., Oefner, C. & Kabsch, W. (1984). Three-dimensional structure of bovine pancreatic DNase I at 2·5 A resolution. EMBO Journal 3, 2423–2430.Google Scholar
Sun, W., Pertzev, A. & Nicholson, A. W. (2005). Catalytic mechanism of Escherichia coli ribonuclease III: kinetic and inhibitor evidence for the involvement of two magnesium ions in RNA phosphodiester hydrolysis. Nucleic Acids Research 33, 807–815.Google Scholar
Syson, K., Tomlinson, C., Chapados, B. R., Sayers, J. R., Tainer, J. A., Williams, N. H. & Grasby, J. A. (2008). Three metal ions participate in the reaction catalyzed by T5 flap endonuclease. Journal of Biological Chemistry 283, 28741–28746.Google Scholar
Szankasi, P. & Smith, G. R. (1995). A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166–1169.Google Scholar
Szankasi, P. & Smith, G. R. (1996). Requirement of S. pombe exonuclease II, a homologue of S. cerevisiae Sep1, for normal mitotic growth and viability. Current Genetics 30, 284–293.Google Scholar
Tadokoro, T. & Kanaya, S. (2009). Ribonuclease H: molecular diversities, substrate binding domains, and catalytic mechanism of the prokaryotic enzymes. FEBS Journal 276, 1482–1493.Google Scholar
Takeuchi, M., Lillis, R., Demple, B. & Takeshita, M. (1994). Interactions of Escherichia coli endonuclease IV and exonuclease III with abasic sites in DNA. Journal of Biological Chemistry 269, 21907–21914.Google Scholar
Tanaka, N., Arai, J., Inokuchi, N., Koyama, T., Ohgi, K., Irie, M. & Nakamura, K. T. (2000). Crystal structure of a plant ribonuclease, RNase LE. Journal of Molecular Biology 298, 859–873.Google Scholar
Thore, S., Mauxion, F., Seraphin, B. & Suck, D. (2003). X-ray structure and activity of the yeast Pop2 protein: a nuclease subunit of the mRNA deadenylase complex. EMBO Reports 4, 1150–1155.Google Scholar
Tock, M. R. & Dryden, D. T. (2005). The biology of restriction and anti-restriction. Current Opinion in Microbiology 8, 466–472.Google Scholar
Tomlinson, C. G., Atack, J. M., Chapados, B., Tainer, J. A. & Grasby, J. A. (2010). Substrate recognition and catalysis by flap endonucleases and related enzymes. Biochemical Society Transactions 38, 433–437.Google Scholar
Ton-Hoang, B., Guynet, C., Ronning, D. R., Cointin-Marty, B., Dyda, F. & Chandler, M. (2005). Transposition of ISHp608, member of an unusual family of bacterial insertion sequences. EMBO Journal 24, 3325–3338.Google Scholar
Toor, N., Keating, K. S. & Pyle, A. M. (2009). Structural insights into RNA splicing. Current Opinion in Structural Biology 19, 260–266.Google Scholar
Toor, N., Rajashankar, K., Keating, K. S. & Pyle, A. M. (2008). Structural basis for exon recognition by a group II intron. Nature Structural and Molecular Biology 15, 1221–1222.Google Scholar
Torres-Larios, A., Swinger, K. K., Pan, T. & Mondragon, A. (2006). Structure of ribonuclease P – a universal ribozyme. Current Opinion in Structural Biology 16, 327–335.Google Scholar
Tran, P. T., Erdeniz, N., Dudley, S. & Liskay, R. M. (2002). Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amsterdam) 1, 895–912.Google Scholar
Truglio, J. J., Rhau, B., Croteau, D. L., Wang, L., Skorvaga, M., Karakas, E., Dellavecchia, M. J., Wang, H., Van Houten, B. & Kisker, C. (2005). Structural insights into the first incision reaction during nucleotide excision repair. EMBO Journal 24, 885–894.Google Scholar
Tsutakawa, S. E., Jingami, H. & Morikawa, K. (1999). Recognition of a TG mismatch: the crystal structure of very short patch repair endonuclease in complex with a DNA duplex. Cell 99, 615–623.Google Scholar
Tucker, P. W., Hazen, E. E. JR. & Cotton, F. A. (1978). Staphylococcal nuclease reviewed: a prototypic study in contemporary enzymology. I. Isolation; physical and enzymatic properties. Molecular and Cellular Biochemistry 22, 67–77.Google Scholar
Uesugi, Y. & Hatanaka, T. (2009). Phospholipase D mechanism using Streptomyces PLD. Biochimica et Biophysica Acta 1791, 962–969.Google Scholar
Unciuleac, M. C. & Shuman, S. (2009). Characterization of the mycobacterial AdnAB DNA motor provides insights into the evolution of bacterial motor-nuclease machines. Journal of Biological Chemistry 285, 2632–2641.Google Scholar
Urakubo, Y., Ikura, T. & Ito, N. (2008). Crystal structural analysis of protein–protein interactions drastically destabilized by a single mutation. Protein Science 17, 1055–1065.Google Scholar
Usui, T., Ohta, T., Oshiumi, H., Tomizawa, J., Ogawa, H. & Ogawa, T. (1998). Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95, 705–716.Google Scholar
Van Gent, D. C., Mizuuchi, K. & Gellert, M. (1996). Similarities between initiation of V(D)J recombination and retroviral integration. Science 271, 1592–1594.Google Scholar
Van Roey, P., Meehan, L., Kowalski, J. C., Belfort, M. & Derbyshire, V. (2002). Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nature Structural Biology 9, 806–811.Google Scholar
Vasu, K., Saravanan, M., Bujnicki, J. M. & Nagaraja, V. (2008). Structural integrity of the beta beta alpha-Metal finger motif is required for DNA binding and stable protein-DNA complex formation in R.KpnI. Biochimica et Biophysica Acta 1784, 269–275.Google Scholar
Verhoeven, E. E., Van Kesteren, M., Moolenaar, G. F., Visse, R. & Goosen, N. (2000). Catalytic sites for 3′ and 5′ incision of Escherichia coli nucleotide excision repair are both located in UvrC. Journal of Biological Chemistry 275, 5120–5123.Google Scholar
Viadiu, H. & Aggarwal, A. K. (1998). The role of metals in catalysis by the restriction endonuclease BamHI. Nature Structural Biology 5, 910–916.Google Scholar
Viadiu, H. & Aggarwal, A. K. (2000). Structure of BamHI bound to nonspecific DNA: a model for DNA sliding. Molecular Cell 5, 889–895.Google Scholar
Vicens, Q. & Cech, T. R. (2006). Atomic level architecture of group I introns revealed. Trends in Biochemical Sciences 31, 41–51.Google Scholar
Viswanathan, M. & Lovett, S. T. (1999). Exonuclease X of Escherichia coli. A novel 3′–5′ DNase and Dnaq superfamily member involved in DNA repair. Journal of Biological Chemistry 274, 30094–30100.Google Scholar
Vitkute, J., Maneliene, Z., Petrusyte, M. & Janulaitis, A. (1998). BfiI, a restriction endonuclease from Bacillus firmus S8120, which recognizes the novel non-palindromic sequence 5′-ACTGGG(N)5/4–3′. Nucleic Acids Research 26, 3348–3349.Google Scholar
Voegtli, W. C., White, D. J., Reiter, N. J., Rusnak, F. & Rosenzweig, A. C. (2000). Structure of the bacteriophage lambda Ser/Thr protein phosphatase with sulfate ion bound in two coordination modes. Biochemistry 39, 15365–15374.Google Scholar
Voet, D. & Voet, J. G. (2004). Biochemistry. Hoboken, NJ: Wiley.Google Scholar
Voziyanov, Y., Pathania, S. & Jayaram, M. (1999). A general model for site-specific recombination by the integrase family recombinases. Nucleic Acids Research 27, 930–941.Google Scholar
Walker, D., Lancaster, L., James, R. & Kleanthous, C. (2004). Identification of the catalytic motif of the microbial ribosome inactivating cytotoxin colicin E3. Protein Sci 13, 1603–1611.Google Scholar
Wang, J. C. (2002). Cellular roles of DNA topoisomerases: a molecular perspective. Nature Reviews Molecular Cell Biology 3, 430–440.Google Scholar
Wang, L. K. & Shuman, S. (2005). Structure-function analysis of yeast tRNA ligase. RNA 11, 966–975.Google Scholar
Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T. & Patel, D. J. (2008). Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921–926.Google Scholar
Wang, Y., Juranek, S., Li, H., Sheng, G., Wardle, G. S., Tuschl, T. & Patel, D. J. (2009). Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754–761.Google Scholar
Wang, Y. T., Yang, W. J., Li, C. L., Doudeva, L. G. & Yuan, H. S. (2007). Structural basis for sequence-dependent DNA cleavage by nonspecific endonucleases. Nucleic Acids Research 35, 584–594.Google Scholar
Wang, Z., Fast, W., Valentine, A. M. & Benkovic, S. J. (1999). Metallo-beta-lactamase: structure and mechanism. Current Opinion in Chemical Biology 3, 614–622.Google Scholar
West, S. C. & Connolly, B. (1992). Biological roles of the Escherichia coli RuvA, RuvB and RuvC proteins revealed. Molecular Microbiology 6, 2755–2759.Google Scholar
Weston, S. A., Lahm, A. & Suck, D. (1992). X-ray structure of the DNase I-d(GGTATACC)2 complex at 2·3 A resolution. Journal of Molecular Biology 226, 1237–1256.Google Scholar
White, M. F. & Lilley, D. M. (1997). Characterization of a Holliday junction-resolving enzyme from Schizosaccharomyces pombe. Molecular Cell Biology 17, 6465–6471.Google Scholar
Widlak, P. (2000). The DFF40/CAD endonuclease and its role in apoptosis. Acta Biochimica Polonica 47, 1037–1044.Google Scholar
Widlak, P. & Garrard, W. T. (2005). Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. Journal of Cellular Biochemistry 94, 1078–1087.Google Scholar
Wiedenheft, B., Zhou, K., Jinek, M., Coyle, S. M., Ma, W. & Doudna, J. A. (2009). Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17, 904–912.Google Scholar
Williams, R. S., Moncalian, G., Williams, J. S., Yamada, Y., Limbo, O., Shin, D. S., Groocock, L. M., Cahill, D., Hitomi, C., Guenther, G., Moiani, D., Carney, J. P., Russell, P. & Tainer, J. A. (2008). Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135, 97–109.Google Scholar
Winkler, F. K., Banner, D. W., Oefner, C., Tsernoglou, D., Brown, R. S., Heathman, S. P., Bryan, R. K., Martin, P. D., Petratos, K. & Wilson, K. S. (1993). The crystal structure of EcoRV endonuclease and of its complexes with cognate and non-cognate DNA fragments. EMBO Journal 12, 1781–1795.Google Scholar
Woo, E. J., Kim, Y. G., Kim, M. S., Han, W. D., Shin, S., Robinson, H., Park, S. Y. & Oh, B. H. (2004). Structural mechanism for inactivation and activation of CAD/DFF40 in the apoptotic pathway. Molecular Cell 14, 531–539.Google Scholar
Worrall, J. A. & Luisi, B. F. (2007). Information available at cut rates: structure and mechanism of ribonucleases. Current Opinion in Structural Biology 17, 128–137.Google Scholar
Wu, M., Reuter, M., Lilie, H., Liu, Y., Wahle, E. & Song, H. (2005). Structural insight into poly(A) binding and catalytic mechanism of human PARN. EMBO Journal 24, 4082–4093.Google Scholar
Wu, S. I., Lo, S. K., Shao, C. P., Tsai, H. W. & Hor, L. I. (2001). Cloning and characterization of a periplasmic nuclease of Vibrio vulnificus and its role in preventing uptake of foreign DNA. Applied and Environmental Microbiology 67, 82–88.Google Scholar
Wyckoff, H. W., Hardman, K. D., Allewell, N. M., Inagami, T., Johnson, L. N. & Richards, F. M. (1967). The structure of ribonuclease-S at 3·5 A resolution. Journal of Biological Chemistry 242, 3984–3988.Google Scholar
Wyckoff, H. W., Tsernoglou, D., Hanson, A. W., Knox, J. R., Lee, B. & Richards, F. M. (1970). The three-dimensional structure of ribonuclease-S. Interpretation of an electron density map at a nominal resolution of 2 A. Journal of Biological Chemistry 245, 305–328.Google Scholar
Xiang, S., Cooper-Morgan, A., Jiao, X., Kiledjian, M., Manley, J. L. & Tong, L. (2009). Structure and function of the 5′→3′ exoribonuclease Rat1 and its activating partner Rai1. Nature 458, 784–788.Google Scholar
Xu, Q. S., Roberts, R. J. & Guo, H. C. (2005). Two crystal forms of the restriction enzyme MspI–DNA complex show the same novel structure. Protein Science 14, 2590–2600.Google Scholar
Xue, S., Calvin, K. & Li, H. (2006). RNA recognition and cleavage by a splicing endonuclease. Science 312, 906–910.Google Scholar
Xue, Y., Bai, X., Lee, I., Kallstrom, G., Ho, J., Brown, J., Stevens, A. & Johnson, A. W. (2000). Saccharomyces cerevisiae RAI1 (YGL246c) is homologous to human DOM3Z and encodes a protein that binds the nuclear exoribonuclease Rat1p. Molecular and Cellular Biology 20, 4006–4015.Google Scholar
Yajima, S., Inoue, S., Ogawa, T., Nonaka, T., Ohsawa, K. & Masaki, H. (2006). Structural basis for sequence-dependent recognition of colicin E5 tRNase by mimicking the mRNA-tRNA interaction. Nucleic Acids Research 34, 6074–6082.Google Scholar
Yakovleva, L., Chen, S., Hecht, S. M. & Shuman, S. (2008). Chemical and traditional mutagenesis of vaccinia DNA topoisomerase provides insights to cleavage site recognition and transesterification chemistry. Journal of Biological Chemistry 283, 16093–16103.Google Scholar
Yamagata, A., Kakuta, Y., Masui, R. & Fukuyama, K. (2002). The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proceedings of the National Academy of Sciences USA 99, 5908–5912.Google Scholar
Yang, K., Zhang, L., Xu, T., Heroux, A. & Zhao, R. (2008). Crystal structure of the beta-finger domain of Prp8 reveals analogy to ribosomal proteins. Proceedings of the National Academy of Sciences USA 105, 13817–13822.Google Scholar
Yang, W. (2007). Human MutLalpha: the jack of all trades in MMR is also an endonuclease. DNA Repair (Amsterdam) 6, 135–139.Google Scholar
Yang, W. (2008). An equivalent metal ion in one- and two-metal-ion catalysis. Nature Structural and Molecular Biology 15, 1228–1231.Google Scholar
Yang, W., Lee, J. Y. & Nowotny, M. (2006). Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Molecular Cell 22, 5–13.Google Scholar
Yang, W. & Mizuuchi, K. (1997). Site-specific recombination in plane view. Structure 5, 1401–1406.Google Scholar
Yang, W. & Steitz, T. A. (1995a). Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell 82, 193–207.Google Scholar
Yang, W. & Steitz, T. A. (1995b). Recombining the structures of HIV integrase, RuvC and RNase H. Structure 3, 131–134.Google Scholar
Yang, X., Gerczei, T., Glover, L. T. & Correll, C. C. (2001). Crystal structures of restrictocin-inhibitor complexes with implications for RNA recognition and base flipping. Nature Structural Biology 8, 968–973.Google Scholar
Yang, X. C., Sullivan, K. D., Marzluff, W. F. & Dominski, Z. (2009). Studies of the 5′ exonuclease and endonuclease activities of CPSF-73 in histone pre-mRNA processing. Molecular and Cellular Biology 29, 31–42.Google Scholar
Yarus, M. (2002). Primordial genetics: phenotype of the ribocyte. Annual Review of Genetics 36, 125–151.Google Scholar
Yoshida, H. (2001). The ribonuclease T1 family. Methods in Enzymology 341, 28–41.Google Scholar
Yoshikawa, M., Iwasaki, H. & Shinagawa, H. (2001). Evidence that phenylalanine 69 in Escherichia coli RuvC resolvase forms a stacking interaction during binding and destabilization of a Holliday junction DNA substrate. Journal of Biological Chemistry 276, 10432–10436.Google Scholar
Yu, M., Souaya, J. & Julin, D. A. (1998). The 30-kDa C-terminal domain of the RecB protein is critical for the nuclease activity, but not the helicase activity, of the RecBCD enzyme from Escherichia coli. Proceedings of the National Academy of Sciences USA 95, 981–986.Google Scholar
Zalatan, J. G., Fenn, T. D. & Herschlag, D. (2008). Comparative enzymology in the alkaline phosphatase superfamily to determine the catalytic role of an active-site metal ion. Journal of Molecular Biology 384, 1174–1189.Google Scholar
Zamel, R., Poon, A., Jaikaran, D., Andersen, A., Olive, J., De Abreu, D. & Collins, R. A. (2004). Exceptionally fast self-cleavage by a Neurospora Varkud satellite ribozyme. Proceedings of the National Academy of Sciences USA 101, 1467–1472.Google Scholar
Zegers, I., Loris, R., Dehollander, G., Fattah Haikal, A., Poortmans, F., Steyaert, J. & Wyns, L. (1998). Hydrolysis of a slow cyclic thiophosphate substrate of RNase T1 analyzed by time-resolved crystallography. Nature Structural Biology 5, 280–283.Google Scholar
Zhang, J., Xing, X., Herr, A. B. & Bell, C. E. (2009). Crystal structure of E. coli RecE protein reveals a toroidal tetramer for processing double-stranded DNA breaks. Structure 17, 690–702.Google Scholar
Zhang, Y., Buchholz, F., Muyrers, J. P. & Stewart, A. F. (1998). A new logic for DNA engineering using recombination in Escherichia coli. Nature Genetics 20, 123–128.Google Scholar
Zhu, C. X. & Tse-Dinh, Y. C. (2000). The acidic triad conserved in type IA DNA topoisomerases is required for binding of Mg(II) and subsequent conformational change. Journal of Biological Chemistry 275, 5318–5322.Google Scholar
Zuo, Y., Vincent, H. A., Zhang, J., Wang, Y., Deutscher, M. P. & Malhotra, A. (2006). Structural basis for processivity and single-strand specificity of RNase II. Molecular Cell 24, 149–156.Google Scholar
Zuo, Y., Wang, Y. & Malhotra, A. (2005). Crystal structure of Escherichia coli RNase D, an exoribonuclease involved in structured RNA processing. Structure 13, 973–984.Google Scholar
Zuo, Y., Zheng, H., Wang, Y., Chruszcz, M., Cymborowski, M., Skarina, T., Savchenko, A., Malhotra, A. & Minor, W. (2007). Crystal structure of RNase T, an exoribonuclease involved in tRNA maturation and end turnover. Structure 15, 417–428.Google Scholar