Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T07:18:28.301Z Has data issue: false hasContentIssue false
  • English
  • Français

Folding of a universal ribozyme: the ribonuclease P RNA

Published online by Cambridge University Press:  12 October 2007

Nathan J. Baird ,
Xing-Wang Fang ,
Narayanan Srividya ,
Tao Pan  and
Tobin R. Sosnick
Nathan J. Baird
Affiliation:
Department of Chemistry, University of Chicago, Chicago, IL 60637, USA Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637, USA
Xing-Wang Fang
Affiliation:
Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637, USA
Narayanan Srividya
Affiliation:
Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637, USA
Tao Pan*
Affiliation:
Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637, USA
Tobin R. Sosnick*
Affiliation:
Institute for Biophysical Dynamics, University of Chicago, Chicago, IL 60637, USA Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL 60637, USA
*
*Correspondence may be addressed to either T. Sosnick or T. Pan at: 929 E. 57th St., Chicago, IL 60637, USA.
*Correspondence may be addressed to either T. Sosnick or T. Pan at: 929 E. 57th St., Chicago, IL 60637, USA.
Get access Rights & Permissions [Opens in a new window]

Abstract

Ribonuclease P is among the first ribozymes discovered, and is the only ubiquitously occurring ribozyme besides the ribosome. The bacterial RNase P RNA is catalytically active without its protein subunit and has been studied for over two decades as a model system for RNA catalysis, structure and folding. This review focuses on the thermodynamic, kinetic and structural frameworks derived from the folding studies of bacterial RNase P RNA.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 40 , Issue 2 , May 2007 , pp. 113 - 161
Copyright
Copyright © Cambridge University Press 2007

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

9. References

Abkevich, V. I., Gutin, A. M. & Shakhnovich, E. I. (1994). Specific nucleus as the transition state for protein folding: evidence from the lattice model. Biochemistry 33, 10026–10036.CrossRefGoogle ScholarPubMed
Altman, S. & Kirsebom, L. (1999). Ribonuclease P. In The RNA World, Second Edition (eds Gesteland, R. F., Cech, T. R. and Atkins, J. F.), pp. 351–380. New York: Cold Spring Harbor Laboratory Press, Cold Spring Harbor.Google Scholar
Baird, N. J., Srividya, N., Krasilnikov, A. S., Mondragon, A., Sosnick, T. R. & Pan, T. (2006). Structural basis for altering the stability of homologous RNAs from a mesophilic and a thermophilic bacterium. RNA 12, 598–606.CrossRefGoogle Scholar
Baird, N. J., Westhof, E., Qin, H., Pan, T. & Sosnick, T. R. (2005). Structure of a folding intermediate reveals the interplay between core and peripheral elements in RNA folding. Journal of Molecular Biology 352, 712–722.CrossRefGoogle ScholarPubMed
Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. (2000). The complete atomic structure of the large ribosomal subunit at 2·4 A resolution. Science 289, 905–920.CrossRefGoogle ScholarPubMed
Bartley, L. E., Zhuang, X., Das, R., Chu, S. & Herschlag, D. (2003). Exploration of the transition state for tertiary structure formation between an RNA helix and a large structured RNA. Journal of Molecular Biology 328, 1011–1026.CrossRefGoogle Scholar
Bassi, G. S., Murchie, A. I., Walter, F., Clegg, R. M. & Lilley, D. M. (1997). Ion-induced folding of the hammerhead ribozyme: a fluorescence resonance energy transfer study. EMBO Journal 16, 7481–7489.CrossRefGoogle ScholarPubMed
Bertone, P., Stolc, V., Royce, T. E., Rozowsky, J. S., Urban, A. E., Zhu, X., Rinn, J. L., Tongprasit, W., Samanta, M., Weissman, S. et al. (2004). Global identification of human transcribed sequences with genome tiling arrays. Science 306, 2242–2246.CrossRefGoogle ScholarPubMed
Bokinsky, G., Rueda, D., Misra, V. K., Rhodes, M. M., Gordus, A., Babcock, H. P., Walter, N. G. & Zhuang, X. (2003). Single-molecule transition-state analysis of RNA folding. Proceedings of the National Academy of Sciences USA 100, 9302–9307.CrossRefGoogle ScholarPubMed
Brown, J. W. (1999). The Ribonuclease P Database. Nucleic Acids Research 27, 314.CrossRefGoogle ScholarPubMed
Brown, J. W., Haas, E. S. & Pace, N. R. (1993). Characterization of ribonuclease P RNAs from thermophilic bacteria. Nucleic Acids Research 21, 671–679.CrossRefGoogle ScholarPubMed
Cantor, C. & Schimmel, P. (1980). Biophysical Chemistry: Part II. New York: W. H. Freeman and Co.Google Scholar
Cate, J. H., Hanna, R. L. & Doudna, J. A. (1997). A magnesium ion core at the heart of a ribozyme domain. Nature Structural Biology 4, 553–558.CrossRefGoogle ScholarPubMed
Celander, D. W. & Cech, T. R. (1991). Visualizing the higher order folding of a catalytic RNA molecule. Science 251, 401–407.CrossRefGoogle ScholarPubMed
Cheng, J., Kapranov, P., Drenkow, J., Dike, S., Brubaker, S., Patel, S., Long, J., Stern, D., Tammana, H., Helt, G. et al. (2005). Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308, 1149–1154.CrossRefGoogle ScholarPubMed
Chin, K., Sharp, K. A., Honig, B. & Pyle, A. M. (1999). Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function. Nature Structural Biology 6, 1055–1061.Google ScholarPubMed
Das, R., Travers, K. J., Bai, Y. & Herschlag, D. (2005). Determining the Mg2+ stoichiometry for folding an RNA metal ion core. Journal of the American Chemical Society 127, 8272–8273.CrossRefGoogle ScholarPubMed
Doherty, E. A. & Doudna, J. A. (1997). The P4-P6 domain directs higher order folding of the Tetrahymena ribozyme core. Biochemistry 36, 3159–3169.CrossRefGoogle ScholarPubMed
Draper, D. E., Grilley, D. & Soto, A. M. (2005). Ions and RNA folding. Annual Review of Biophysics and Biomolecular Structures 34, 221–243.CrossRefGoogle ScholarPubMed
Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J. P. & Ehresmann, B. (1987). Probing the structure of RNAs in solution. Nucleic Acids Research 15, 9109–9128.CrossRefGoogle ScholarPubMed
Fang, X., Littrell, K., Yang, X., Henderson, S. J., Siefert, S., Thiyagarajan, P., Pan, T. & Sosnick, T. R. (2000). Mg2+-dependent compaction and folding of yeast tRNA(Phe) and the catalytic domain of the B. subtilis RNase P RNA determined by small-angle X-ray scattering. Biochemistry 39, 11107–11113.CrossRefGoogle Scholar
Fang, X., Pan, T. & Sosnick, T. R. (1999a). Mg2+-dependent folding of a large ribozyme without kinetic traps. Nature Structural Biology 6, 1091–1095.Google ScholarPubMed
Fang, X., Pan, T. & Sosnick, T. R. (1999b). A thermodynamic framework and cooperativity in the tertiary folding of a Mg2+-dependent ribozyme. Biochemistry 38, 16840–16846.CrossRefGoogle ScholarPubMed
Fang, X. W., Golden, B. L., Littrell, K., Shelton, V., Thiyagarajan, P., Pan, T. & Sosnick, T. R. (2001). The thermodynamic origin of the stability of a thermophilic ribozyme. Proceedings of the National Academy of Sciences USA 98, 4355–4360.CrossRefGoogle ScholarPubMed
Fang, X. W., Thiyagarajan, P., Sosnick, T. R. & Pan, T. (2002). The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proceedings of the National Academy of Sciences USA 99, 8518–8523.CrossRefGoogle ScholarPubMed
Feng, H., Vu, N. D., Zhou, Z. & Bai, Y. (2004). Structural examination of Phi value analysis in protein folding. Biochemistry 43, 14325–14331.CrossRefGoogle ScholarPubMed
Fenley, M. O., Manning, G. S. & Olson, W. K. (1990). Approach to the limit of counterion condensation. Biopolymers 30, 1191–1203.CrossRefGoogle Scholar
Ferre-D'Amare, A. R., Zhou, K. & Doudna, J. A. (1998). Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567–574.CrossRefGoogle ScholarPubMed
Fersht, A. R., Matouschek, A. & Serrano, L. (1992). The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. Journal of Molecular Biology 224, 771–782.CrossRefGoogle ScholarPubMed
Frank, D. N. & Pace, N. R. (1998). Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annual Review of Biochemistry 67, 153–180.CrossRefGoogle Scholar
Galtier, N. & Lobry, J. R. (1997). Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. Journal of Molecular Evolution 44, 632–636.CrossRefGoogle ScholarPubMed
Goldenberg, D. P. (1992). Mutational analysis of protein folding and stability. In Protein Folding (ed. Creighton, T. E.), pp. 353–403. New York: W. H. Freeman.Google Scholar
Gray, D. M., Hung, S. H. & Johnson, K. H. (1995). Absorption and circular dichroism spectroscopy of nucleic acid duplexes and triplexes. Methods in Enzymology 246, 19–34.CrossRefGoogle ScholarPubMed
Guo, F. & Cech, T. R. (2002). Evolution of Tetrahymena ribozyme mutants with increased structural stability. Nature Structural Biology 9, 855–861.Google ScholarPubMed
Guo, Z. Y. & Thirumalai, D. (1995). Kinetics of protein-folding: nucleation mechanism, time scales, and pathways. Biopolymers 36, 83–102.CrossRefGoogle Scholar
Ha, T., Zhuang, X., Kim, H. D., Orr, J. W., Williamson, J. R. & Chu, S. (1999). Ligand-induced conformational changes observed in single RNA molecules. Proceedings of the National Academy of Sciences USA 96, 9077–9082.CrossRefGoogle ScholarPubMed
Heilman-Miller, S. L., Thirumalai, D. & Woodson, S. A. (2001). Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations. Journal of Molecular Biology 306, 1157–1166.CrossRefGoogle ScholarPubMed
Heilman-Miller, S. L. & Woodson, S. A. (2003). Perturbed folding kinetics of circularly permuted RNAs with altered topology. Journal of Molecular Biology 328, 385–394.CrossRefGoogle ScholarPubMed
Helm, L. & Hertz, H. G. (1981). The hydration of the alkaline earth metal ions Mg2+, Ca2+, Sr2+ and Ba2+, a nuclear magnetic relaxation study involving the quadrupole moment of the ionic nuclei. Zeitschrift für Physikalische Chemie 127, 23–44.CrossRefGoogle Scholar
Hermann, T. & Westhof, E. (1998). Exploration of metal ion binding sites in RNA folds by Brownian-dynamics simulations. Structure 6, 1303–1314.CrossRefGoogle ScholarPubMed
Jovine, L., Djordjevic, S. & Rhodes, D. (2000). The crystal structure of yeast phenylalanine tRNA at 2·0 A resolution: cleavage by Mg2+ in 15-year-old crystals. Journal of Molecular Biology 301, 401–414.CrossRefGoogle Scholar
Kapranov, P., Cawley, S. E., Drenkow, J., Bekiranov, S., Strausberg, R. L., Fodor, S. P. & Gingeras, T. R. (2002). Large-scale transcriptional activity in chromosomes 21 and 22. Science 296, 916–919.CrossRefGoogle Scholar
Kazantsev, A. V., Krivenko, A. A., Harrington, D. J., Holbrook, S. R., Adams, P. D. & Pace, N. R. (2005). Crystal structure of a bacterial ribonuclease P RNA. Proceedings of the National Academy of Sciences USA 102, 13392–13397.CrossRefGoogle ScholarPubMed
Kent, O., Chaulk, S. G. & MacMillan, A. M. (2000). Kinetic analysis of the M1 RNA folding pathway. Journal of Molecular Biology 304, 699–705.CrossRefGoogle ScholarPubMed
Kim, H. D., Nienhaus, G. U., Ha, T., Orr, J. W., Williamson, J. R. & Chu, S. (2002). Mg2+-dependent conformational change of RNA studied by fluorescence correlation and FRET on immobilized single molecules. Proceedings of the National Academy of Sciences USA 99, 4284–4289.CrossRefGoogle ScholarPubMed
Klein, D. J., Moore, P. B. & Steitz, T. A. (2004). The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10, 1366–1379.CrossRefGoogle Scholar
Kowalak, J. A., Dalluge, J. J., McCloskey, J. A. & Stetter, K. O. (1994). The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 33, 7869–7876.CrossRefGoogle ScholarPubMed
Krantz, B. A., Dothager, R. S. & Sosnick, T. R. (2004). Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. Journal of Molecular Biology 337, 463–475.CrossRefGoogle ScholarPubMed
Krantz, B. A., Moran, L. B., Kentsis, A. & Sosnick, T. R. (2000). D/H amide kinetic isotope effects reveal when hydrogen bonds form during protein folding. Nature Structural Biology 7, 62–71.Google ScholarPubMed
Krantz, B. A. & Sosnick, T. R. (2001). Engineered metal binding sites map the heterogeneous folding landscape of a coiled coil. Nature Structural Biology 8, 1042–1047.CrossRefGoogle ScholarPubMed
Krantz, B. A., Srivastava, A. K., Nauli, S., Baker, D., Sauer, R. T. & Sosnick, T. R. (2002). Understanding protein hydrogen bond formation with kinetic H/D amide isotope effects. Nature Structural Biology 9, 458–463.CrossRefGoogle ScholarPubMed
Krasilnikov, A. S., Xiao, Y., Pan, T. & Mondragon, A. (2004). Basis for structural diversity in homologous RNAs. Science 306, 104–107.CrossRefGoogle ScholarPubMed
Krasilnikov, A. S., Yang, X., Pan, T. & Mondragon, A. (2003). Crystal structure of the specificity domain of ribonuclease P. Nature 421, 760–764.CrossRefGoogle ScholarPubMed
Laing, L. G., Gluick, T. C. & Draper, D. E. (1994). Stabilization of RNA structure by Mg ions. Specific and non-specific effects. Journal of Molecular Biology 237, 577–587.CrossRefGoogle ScholarPubMed
Latham, J. A. & Cech, T. R. (1989). Defining the inside and outside of a catalytic RNA molecule. Science 245, 276–282.CrossRefGoogle ScholarPubMed
Liphardt, J., Onoa, B., Smith, S. B., Tinoco, I. J. & Bustamante, C. (2001). Reversible unfolding of single RNA molecules by mechanical force. Science 292, 733–737.CrossRefGoogle ScholarPubMed
Loria, A. & Pan, T. (1996). Domain structure of the ribozyme from eubacterial ribonuclease P. RNA 2, 551–563.Google ScholarPubMed
Manning, G. S. (1978). Limiting laws and counterion condensation in polyelectrolyte solutions. V. Further development of the chemical model. Biophysical Chemistry 9, 65–70.CrossRefGoogle ScholarPubMed
Massire, C., Jaeger, L. & Westhof, E. (1998). Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. Journal of Molecular Biology 279, 773–793.CrossRefGoogle ScholarPubMed
Matthews, C. R. (1987). Effects of point mutations on the folding of globular proteins. Methods in Enzymology 154, 498–511.CrossRefGoogle ScholarPubMed
Misra, V. K. & Draper, D. E. (2000). Mg2+ binding to tRNA revisited: the nonlinear Poisson-Boltzmann model. Journal of Molecular Biology 299, 813–825.CrossRefGoogle ScholarPubMed
Misra, V. K. & Draper, D. E. (2002). The linkage between magnesium binding and RNA folding. Journal of Molecular Biology 317, 507–521.CrossRefGoogle ScholarPubMed
Misra, V. K., Shiman, R. & Draper, D. E. (2003). A thermodynamic framework for the magnesium-dependent folding of RNA. Biopolymers 69, 118–136.CrossRefGoogle ScholarPubMed
Moore, M. J. & Sharp, P. A. (1992). Site-specific modification of pre-mRNA: the 2′-hydroxyl groups at the splice sites. Science 256, 992–997.CrossRefGoogle Scholar
Myers, J. K., Pace, C. N. & Scholtz, J. M. (1995). Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Science 4, 2138–2148.CrossRefGoogle ScholarPubMed
Pace, C. N. (1986). Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods in Enzymology 131, 266–280.CrossRefGoogle ScholarPubMed
Pan, J., Thirumalai, D. & Woodson, S. A. (1997). Folding of RNA involves parallel pathways. Journal of Molecular Biology 273, 7–13.CrossRefGoogle ScholarPubMed
Pan, T. (1995a). Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry 34, 902–909.CrossRefGoogle ScholarPubMed
Pan, T. (1995b). Novel RNA substrates for the ribozyme from Bacillus subtilis ribonuclease P identified by in vitro selection. Biochemistry 34, 8458–8464.CrossRefGoogle ScholarPubMed
Pan, T. (2000). Probing RNA structure and function using circular permutation. Methods in Enzymology 317, 313–330.CrossRefGoogle ScholarPubMed
Pan, T., Artsimovitch, I., Fang, X., Landick, R. & Sosnick, T. R. (1999a). Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proceedings of the National Academy of Sciences USA 96, 9545–9550.CrossRefGoogle ScholarPubMed
Pan, T., Fang, X. & Sosnick, T. R. (1999b). Pathway modulation, circular permutation and rapid RNA folding under kinetic control. Journal of Molecular Biology 286, 721–731.CrossRefGoogle ScholarPubMed
Pan, T. & Jakacka, M. (1996). Multiple substrate binding sites in the ribozyme from Bacillus subtilis RNase P. EMBO Journal 15, 2249–2255.CrossRefGoogle ScholarPubMed
Pan, T. & Sosnick, T. (2006). RNA folding during transcription. Annual Review of Biophysics and Biomolecular Structures 35, 161–175.CrossRefGoogle ScholarPubMed
Pan, T. & Sosnick, T. R. (1997). Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nature Structural Biology 4, 931–938.CrossRefGoogle ScholarPubMed
Plaxco, K. W., Simons, K. T. & Baker, D. (1998). Contact order, transition state placement and the refolding rates of single domain proteins. Journal of Molecular Biology 277, 985–994.CrossRefGoogle ScholarPubMed
Plaxco, K. W., Simons, K. T., Ruczinski, I. & Baker, D. (2000). Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry 39, 11177–11183.CrossRefGoogle ScholarPubMed
Puglisi, J. D. & Jr.Tinoco, I. (1989). Absorbance melting curves of RNA. Methods in Enzymology 180, 304–325.CrossRefGoogle ScholarPubMed
Qin, H., Sosnick, T. R. & Pan, T. (2001). Modular construction of a tertiary RNA structure: the specificity domain of the Bacillus subtilis RNase P RNA. Biochemistry 40, 11202–11210.CrossRefGoogle ScholarPubMed
Rupert, P. B. & Ferre-D'Amare, A. R. (2001). Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410, 780–786.CrossRefGoogle ScholarPubMed
Russell, R., Zhuang, X., Babcock, H. P., Millett, I. S., Doniach, S., Chu, S. & Herschlag, D. (2002). Exploring the folding landscape of a structured RNA. Proceedings of the National Academy of Sciences USA 99, 155–160.CrossRefGoogle ScholarPubMed
Jr.SantaLucia, J., Kierzek, R. & Turner, D. H. (1990). Effects of GA mismatches on the structure and thermodynamics of RNA internal loops. Biochemistry 29, 8813–8819.CrossRefGoogle ScholarPubMed
Sclavi, B., Woodson, S., Sullivan, M., Chance, M. R. & Brenowitz, M. (1997). Time-resolved synchrotron X-ray ‘footprinting’, a new approach to the study of nucleic acid structure and function: application to protein-DNA interactions and RNA folding. Journal of Molecular Biology 266, 144–159.CrossRefGoogle Scholar
Seifert, S., Winans, R. E., Tiede, D. M. & Thiyagarajan, P. (2000). Design and performance of a ASAXS instrument at the Advanced Photon Source. Journal of Applied Crystallography 33, 782–784.CrossRefGoogle Scholar
Shelton, V. M., Sosnick, T. R. & Pan, T. (1999). Applicability of urea in the thermodynamic analysis of secondary and tertiary RNA folding. Biochemistry 38, 16831–16839.CrossRefGoogle ScholarPubMed
Shi, H. & Moore, P. B. (2000). The crystal structure of yeast phenylalanine tRNA at 1·93 A resolution: a classic structure revisited. RNA 6, 1091–1105.CrossRefGoogle ScholarPubMed
Silverman, S. K. & Cech, T. R. (2001). An early transition state for folding of the P4-P6 RNA domain. RNA 7, 161–166.CrossRefGoogle ScholarPubMed
Sosnick, T. R., Dothager, R. S. & Krantz, B. A. (2004). Differences in the folding transition state of ubiquitin indicated by phi and psi analyses. Proceedings of the National Academy of Sciences USA 101, 17377–17382.CrossRefGoogle ScholarPubMed
Sosnick, T. R., Fang, X. & Shelton, V. M. (2000). Application of circular dichroism to study RNA folding transitions. Methods in Enzymology 317, 393–409.CrossRefGoogle ScholarPubMed
Sosnick, T. R., Mayne, L. & Englander, S. W. (1996). Molecular collapse: The rate-limiting step in two-state cytochrome c folding. Proteins 24, 413–426.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
Sosnick, T. R. & Pan, T. (2003). RNA folding: models and perspectives. Current Opinion in Structural Biology 13, 309–316.CrossRefGoogle Scholar
Sosnick, T. R. & Pan, T. (2004). Reduced contact order and RNA folding rates. Journal of Molecular Biology 342, 1359–1365.CrossRefGoogle ScholarPubMed
Stolc, V., Gauhar, Z., Mason, C., Halasz, G., van Batenburg, M. F., Rifkin, S. A., Hua, S., Herreman, T., Tongprasit, W., Barbano, P. E., et al. (2004). A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306, 655–660.CrossRefGoogle ScholarPubMed
Svergun, D. I. & Koch, M. H. J. (2003). Small-angle scattering studies of biological macromolecules in solution. Reports on Progress in Physics 66, 1735–1782.CrossRefGoogle Scholar
Swisher, J. F., Su, L. J., Brenowitz, M., Anderson, V. E. & Pyle, A. M. (2002). Productive folding to the native state by a group II intron ribozyme. Journal of Molecular Biology 315, 297–310.CrossRefGoogle Scholar
Thirumalai, D. & Hyeon, C. (2005). RNA and protein folding: common themes and variations. Biochemistry 44, 4957–4970.CrossRefGoogle ScholarPubMed
Torres-Larios, A., Swinger, K. K., Krasilnikov, A. S., Pan, T. & Mondragon, A. (2005). Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437, 584–587.CrossRefGoogle ScholarPubMed
Treiber, D. K., Rook, M. S., Zarrinkar, P. P. & Williamson, J. R. (1998). Kinetic intermediates trapped by native interactions in RNA folding. Science 279, 1943–1946.CrossRefGoogle ScholarPubMed
Treiber, D. K. & Williamson, J. R. (2001). Beyond kinetic traps in RNA folding. Current Opinion in Structural Biology 11, 309–314.CrossRefGoogle ScholarPubMed
Turner, D. H. & Sugimoto, N. (1988). RNA structure prediction. Annual Review of Biophysics and Biophysical Chemistry 17, 167–192.CrossRefGoogle ScholarPubMed
Walter, F., Murchie, A. I. H. & Lilley, D. M. J. (1998). Folding of the four-way RNA junction of the hairpin ribozyme. Biochemistry 37, 17629–17636.CrossRefGoogle ScholarPubMed
Wong, T., Sosnick, T. R. & Pan, T. (2005). Mechanistic insights on the folding of a large ribozyme during transcription. Biochemistry 44, 7535–7342.CrossRefGoogle ScholarPubMed
Woodson, S. A. (2002). Folding mechanisms of group I ribozymes: role of stability and contact order. Biochemical Society Transactions 30, 1166–1169.CrossRefGoogle Scholar
Woodson, S. A. (2005). Metal ions and RNA folding: a highly charged topic with a dynamic future. Current Opinion in Chemical Biology 9, 104–109.CrossRefGoogle ScholarPubMed
Woody, R. W. (1995). Circular dichroism. Methods in Enzymology 246, 34–71.CrossRefGoogle ScholarPubMed
Xie, Z., Srividya, N., Sosnick, T. R., Pan, T. & Scherer, N. F. (2004). Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. Proceedings of the National Academy of Sciences USA 101, 534–539.CrossRefGoogle ScholarPubMed
Zarrinkar, P. P., Wang, J. & Williamson, J. R. (1996). Slow folding kinetics of RNase P RNA. RNA 2, 564–573.Google ScholarPubMed
Zarrinkar, P. P. & Williamson, J. R. (1996). The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding [see comments]. Nature Structural Biology 3, 432–438.CrossRefGoogle ScholarPubMed
Zhuang, X., Bartley, L. E., Babcock, H. P., Russell, R., Ha, T., Herschlag, D. & Chu, S. (2000). A single-molecule study of RNA catalysis and folding. Science 288, 2048–2051.CrossRefGoogle ScholarPubMed
Zhuang, X., Kim, H., Pereira, M. J., Babcock, H. P., Walter, N. G. & Chu, S. (2002). Correlating structural dynamics and function in single ribozyme molecules. Science 296, 1473–1476.CrossRefGoogle ScholarPubMed