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Nuclease colicins and their immunity proteins

Published online by Cambridge University Press:  16 November 2011

Grigorios Papadakos ,
Justyna A. Wojdyla  and
Colin Kleanthous
Grigorios Papadakos
Affiliation:
Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK
Justyna A. Wojdyla
Affiliation:
Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK
Colin Kleanthous*
Affiliation:
Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK
*
*Address for correspondence: Professor C. Kleanthous, Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK. Tel.: +44-1904-328820; Fax: +44-1904-328825; Email: [email protected]
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Abstract

It is more than 80 years since Gratia first described ‘a remarkable antagonism between two strains of Escherichia coli’. Shown subsequently to be due to the action of proteins (or peptides) produced by one bacterium to kill closely related species with which it might be cohabiting, such bacteriocins have since been shown to be commonplace in the internecine warfare between bacteria. Bacteriocins have been studied primarily from the twin perspectives of how they shape microbial communities and how they penetrate bacteria to kill them. Here, we review the modes of action of a family of bacteriocins that cleave nucleic acid substrates in E. coli, known collectively as nuclease colicins, and the specific immunity (inhibitor) proteins that colicin-producing organisms make in order to avoid committing suicide. In a process akin to targeting in mitochondria, nuclease colicins engage in a variety of cellular associations in order to translocate their cytotoxic domains through the cell envelope to the cytoplasm. As well as informing on the process itself, the study of nuclease colicin import has also illuminated functional aspects of the host proteins they parasitize. We also review recent studies where nuclease colicins and their immunity proteins have been used as model systems for addressing fundamental problems in protein folding and protein–protein interactions, areas of biophysics that are intimately linked to the role of colicins in bacterial competition and to the import process itself.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 45 , Issue 1 , February 2012 , pp. 57 - 103
Copyright
Copyright © Cambridge University Press 2011

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References

11. References

Anderluh, G., Hong, Q., Boetzel, R., Macdonald, C., Moore, G. R., Virden, R. & Lakey, J. H. (2003). Concerted folding and binding of a flexible colicin domain to its periplasmic receptor TolA. Journal of Biological Chemistry 278, 21860–21868.CrossRefGoogle ScholarPubMed
Anderluh, G. & Lakey, J. H. (2008). Disparate proteins use similar architectures to damage membranes. Trends in Biochemical Sciences 33, 482–490.CrossRefGoogle ScholarPubMed
Arnold, T., Zeth, K. & Linke, D. (2009). Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. Journal of Biological Chemistry 284, 6403–6413.CrossRefGoogle ScholarPubMed
Baboolal, T. G., Conroy, M. J., Gill, K., Ridley, H., Visudtiphole, V., Bullough, P. A. & Lakey, J. H. (2008). Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F. Structure 16, 371–379.CrossRefGoogle Scholar
Baldwin, R. L., Frieden, C. & Rose, G. D. (2010). Dry molten globule intermediates and the mechanism of protein unfolding. Proteins 78, 2725–2737.CrossRefGoogle ScholarPubMed
Barneoud-Arnoulet, A., Barreteau, H., Touze, T., Mengin-Lecreulx, D., Lloubes, R. & Duche, D. (2010a). Toxicity of the colicin M catalytic domain exported to the periplasm is FkpA independent. Journal of Bacteriology 192, 5212–5219.CrossRefGoogle Scholar
Barneoud-Arnoulet, A., Gavioli, M., Lloubes, R. & Cascales, E. (2010b). Interaction of the colicin K bactericidal toxin with components of its import machinery in the periplasm of Escherichia coli. Journal of Bacteriology 192, 5934–5942.CrossRefGoogle ScholarPubMed
Baron, R., Wong, S. E., De Oliveira, C. A. & Mccammon, J. A. (2008). E9-Im9 colicin DNase-immunity protein biomolecular association in water: a multiple-copy and accelerated molecular dynamics simulation study. Journal of Physical Chemistry B 112, 16802–16814.CrossRefGoogle Scholar
Barreteau, H., Bouhss, A., Gerard, F., Duche, D., Boussaid, B., Blanot, D., Lloubes, R., Mengin-Lecreulx, D. & Touze, T. (2010). Deciphering the catalytic domain of colicin M, a peptidoglycan lipid II-degrading enzyme. Journal of Biological Chemistry 285, 12378–12389.CrossRefGoogle ScholarPubMed
Benedetti, H., Frenette, M., Baty, D., Knibiehler, M., Pattus, F. & Lazdunski, C. (1991). Individual domains of colicins confer specificity in colicin uptake, in pore-properties and in immunity requirement. Journal of Molecular Biology 217, 429–439.CrossRefGoogle ScholarPubMed
Benedetti, H., Lloubes, R., Lazdunski, C. & Letellier, L. (1992). Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore has formed. EMBO Journal 11, 441–447.CrossRefGoogle ScholarPubMed
Beppu, T., Kawabata, K. & Arima, K. (1972). Specific inhibition of cell division by colicin E2 without degradation of deoxyribonucleic acid in a new colicin sensitivity mutant of Escherichia coli. Journal of Bacteriology 110, 485–493.CrossRefGoogle Scholar
Bernath, K., Magdassi, S. & Tawfik, D. S. (2005). Directed evolution of protein inhibitors of DNA-nucleases by in vitro compartmentalization (IVC) and nano-droplet delivery. Journal of Molecular Biology 345, 1015–1026.CrossRefGoogle ScholarPubMed
Bonsor, D. A., Grishkovskaya, I., Dodson, E. J. & Kleanthous, C. (2007). Molecular mimicry enables competitive recruitment by a natively disordered protein. Journal of the American Chemical Society 15, 4800–4807.CrossRefGoogle Scholar
Bonsor, D. A., Hecht, O., Vankemmelbeke, M., Sharma, A., Krachler, A. M., Housden, N. G., Lilly, K. J., James, R., Moore, G. R. & Kleanthous, C. (2009a). Allosteric β-propeller signalling in TolB and its manipulation by translocating colicins. EMBO Journal 28, 2846–2857.CrossRefGoogle ScholarPubMed
Bonsor, D. A., Hecht, O., Vankemmelbeke, M., Sharma, A., Krachler, A. M., Housden, N. G., Lilly, K. J., James, R., Moore, G. R. & Kleanthous, C. (2009b). Allosteric beta-propeller signalling in TolB and its manipulation by translocating colicins. EMBO Journal 28, 2846–2857.CrossRefGoogle ScholarPubMed
Bourdineaud, J. P., Boulanger, P., Lazdunski, C. & Letellier, L. (1990a). In vivo properties of colicin A: channel activity is voltage dependent but translocation may be voltage independent. Proceedings of the National Academy of Sciences, U. S. A. 87(3), 1037.CrossRefGoogle ScholarPubMed
Bourdineaud, J. P., Fierobe, H. P., Lazdunski, C. & Pages, J. M. (1990b). Involvement of OmpF during reception and translocation steps of colicin N entry. Molecular Microbiology 4, 1737–1743.CrossRefGoogle ScholarPubMed
Bouveret, E., Benedetti, H., Rigal, A., Loret, E. & Lazdunski, C. (1999). In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. Journal of Bacteriology 181, 6306–6311.CrossRefGoogle ScholarPubMed
Bouveret, E., Rigal, A., Lazdunski, C. & Benedetti, H. (1998). Distinct regions of the colicin A translocation domain are involved in the interaction with TolA and TolB proteins upon import into Escherichia coli. Molecular Microbiology 27, 143–157.CrossRefGoogle ScholarPubMed
Buchanan, S. K., Lukacik, P., Grizot, S., Ghirlando, R., Ali, M. M., Barnard, T. J., Jakes, K. S., Kienker, P. K. & Esser, L. (2007). Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO Journal 26, 2594–2604.CrossRefGoogle Scholar
Cadieux, N., Phan, P. G., Cafiso, D. S. & Kadner, R. J. (2003). Differential substrate-induced signaling through the TonB-dependent transporter BtuB. Proceedings of the National Academy of Sciences, U. S. A. 100, 10688–10693.CrossRefGoogle ScholarPubMed
Capaldi, A. P., Kleanthous, C. & Radford, S. E. (2002). Im7 folding mechanism: misfolding on a path to the native state. Nature Structural Biology 9, 209–216.Google Scholar
Capaldi, A. P., Shastry, M. C., Kleanthous, C., Roder, H. & Radford, S. E. (2001). Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nature Structural Biology 8, 68–72.Google ScholarPubMed
Carr, S., Walker, D., James, R., Kleanthous, C. & Hemmings, A. M. (2000). Crystallization of the cytotoxic domain of a ribosome-inactivating colicin in complex with its immunity protein. Acta Crystallographica. Section D, Biological Crystallography 56, 1630–1633.CrossRefGoogle ScholarPubMed
Cascales, E., Buchanan, S. K., Duche, D., Kleanthous, C., Lloubes, R., Postle, K., Riley, M., Slatin, S. & Cavard, D. (2007). Colicin biology. Microbiology and Molecular Biology Review 71, 158–229.CrossRefGoogle ScholarPubMed
Cascales, E., Gavioli, M., Sturgis, J. N. & Lloubes, R. (2000). Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Molecular Microbiology 38, 904–915.CrossRefGoogle ScholarPubMed
Cascales, E., Lloubes, R. & Sturgis, J. N. (2001). The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA–MotB. Molecular Microbiology 42, 795–807.CrossRefGoogle ScholarPubMed
Cavard, D. & Lazdunski, C. (1990). Colicin cleavage by OmpT protease during both entry into and release from Escherichia coli cells. Journal of Bacteriology 172, 648–652.CrossRefGoogle ScholarPubMed
Chauleau, M., Mora, L., Serba, J. & De Zamaroczy, M. (2011). FtsH-dependent processing of RNase colicins D and E3 means that only the cytotoxic domains are imported into the cytoplasm. Journal of Biological Chemistry 286, 29397–29407.CrossRefGoogle ScholarPubMed
Cobos, E. S. & Radford, S. E. (2006). Sulfate-induced effects in the on-pathway intermediate of the bacterial immunity protein Im7. Biochemistry 45, 2274–2282.CrossRefGoogle ScholarPubMed
Collins, E. S., Whittaker, S. B., Tozawa, K., Macdonald, C., Boetzel, R., Penfold, C. N., Reilly, A., Clayden, N. J., Osborne, M. J., Hemmings, A. M., Kleanthous, C., James, R. & Moore, G. R. (2002). Structural dynamics of the membrane translocation domain of colicin E9 and its interaction with TolB. Journal of Molecular Biology 318, 787–904.CrossRefGoogle ScholarPubMed
Cramer, W. A., Zhang, Y. L., Schendel, S., Merrill, A. R., Song, H. Y., Stauffacher, C. V. & Cohen, F. S. (1992). Dynamic properties of the colicin E1 ion channel. FEMS Microbiology and Immunology 5, 71–81.CrossRefGoogle ScholarPubMed
Cranz-Mileva, S., Friel, C. T. & Radford, S. E. (2005). Helix stability and hydrophobicity in the folding mechanism of the bacterial immunity protein Im9. Protein Engineering, Design and Selection 18, 41–50.CrossRefGoogle ScholarPubMed
Davies, J. K. & Reeves, P. (1975a). Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. Journal of Bacteriology 123, 102–117.CrossRefGoogle ScholarPubMed
Davies, J. K. & Reeves, P. (1975b). Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. Journal of Bacteriology 123, 96–101.CrossRefGoogle ScholarPubMed
De Zamaroczy, M. & Buckingham, R. H. (2002). Importation of nuclease colicins into E coli cells: endoproteolytic cleavage and its prevention by the immunity protein. Biochimie 84, 423–432.CrossRefGoogle ScholarPubMed
De Zamaroczy, M., Mora, L., Lecuyer, A., Geli, V. & Buckingham, R. H. (2001). Cleavage of colicin D is necessary for cell killing and requires the inner membrane peptidase LepB. Molecular Cell 8, 159–168.CrossRefGoogle ScholarPubMed
Dennis, C. A., Videler, H., Pauptit, R. A., Wallis, R., James, R., Moore, G. R. & Kleanthous, C. (1998). A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochemistry Journal 333, 183–191.CrossRefGoogle ScholarPubMed
Deprez, C., Blanchard, L., Guerlesquin, F., Gavioli, M., Simorre, J. P., Lazdunski, C., Marion, D. & Lloubes, R. (2002). Macromolecular import into Escherichia coli: the TolA C-terminal domain changes conformation when interacting with the colicin A toxin. Biochemistry 41, 2589–2598.CrossRefGoogle ScholarPubMed
Derouiche, R., Zeder-Lutz, G., Benedetti, H., Gavioli, M., Rigal, A., Lazdunskil, C. & Lloubes, R. (1997). Binding of colicins A and E1 to purified TolA domains. Microbiology 143, 3185–3192.CrossRefGoogle Scholar
Doudeva, L. G., Huang, H., Hsia, K. C., Shi, Z., Li, C. L., Shen, Y., Cheng, Y. S. & Yuan, H. S. (2006). Crystal structural analysis and metal-dependent stability and activity studies of the ColE7 endonuclease domain in complex with DNA/Zn2+ or inhibitor/Ni2+. Protein Science 15, 269–280.CrossRefGoogle ScholarPubMed
Duche, D., Baty, D., Chartier, M. & Letellier, L. (1994). Unfolding of colicin A during its translocation through the Escherichia coli envelope as demonstrated by disulfide bond engineering. Journal of Biological Chemistry 269, 24820.CrossRefGoogle ScholarPubMed
Duche, D., Frenkian, A., Prima, V. & Lloubes, R. (2006). Release of immunity protein requires functional endonuclease colicin import machinery. Journal of Bacteriology 188, 8593–8600.CrossRefGoogle ScholarPubMed
Duche, D., Issouf, M. & Lloubes, R. (2009). Immunity protein protects colicin E2 from OmpT protease. Journal of Biochemistry 145, 95–101.CrossRefGoogle ScholarPubMed
El Ghachi, M., Bouhss, A., Barreteau, H., Touze, T., Auger, G., Blanot, D. & Mengin-Lecreulx, D. (2006). Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. Journal of Biological Chemistry 281, 22761–22772.CrossRefGoogle ScholarPubMed
El Kouhen, R., Fierobe, H. P., Scianimanico, S., Steiert, M., Pattus, F. & Pages, J. M. (1993). Characterization of the receptor and translocator domains of colicin N. European Journal of Biochemistry 214, 635–639.CrossRefGoogle ScholarPubMed
Ferguson, N., Capaldi, A. P., James, R., Kleanthous, C. & Radford, S. E. (1999). Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. Journal of Molecular Biology 286, 1597–1608.CrossRefGoogle ScholarPubMed
Ferguson, N., Li, W., Capaldi, A. P., Kleanthous, C. & Radford, S. E. (2001). Using chimeric immunity proteins to explore the energy landscape for alpha-helical protein folding. Journal of Molecular Biology 307, 393–405.CrossRefGoogle ScholarPubMed
Foit, L., Morgan, G. J., Kern, M. J., Steimer, L. R., Von Hacht, A. A., Titchmarsh, J., Warriner, S. L., Radford, S. E. & Bardwell, J. C. (2009). Optimizing protein stability in vivo. Molecular Cell 36, 861–871.CrossRefGoogle ScholarPubMed
Friel, C. T., Beddard, G. S. & Radford, S. E. (2004). Switching two-state to three-state kinetics in the helical protein Im9 via the optimisation of stabilising non-native interactions by design. Journal of Molecular Biology 342, 261–273.CrossRefGoogle ScholarPubMed
Friel, C. T., Capaldi, A. P. & Radford, S. E. (2003). Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: similarities and differences in the folding of homologous proteins. Journal of Molecular Biology 326, 293–305.CrossRefGoogle ScholarPubMed
Friel, C. T., Smith, D. A., Vendruscolo, M., Gsponer, J. & Radford, S. E. (2009). The mechanism of folding of Im7 reveals competition between functional and kinetic evolutionary constraints. Nature Structural and Molecular Biology 16, 318–324.CrossRefGoogle ScholarPubMed
Galburt, E. A. & Stoddard, B. L. (2002). Catalytic mechanisms of restriction and homing endonucleases. Biochemistry 41, 13851–13860.CrossRefGoogle ScholarPubMed
Gardner, A., West, S. A. & Buckling, A. (2004). Bacteriocins, spite and virulence. Proceedings of the Royal Society of London B 271, 1529–1535.CrossRefGoogle ScholarPubMed
Gerard, F., Brooks, M. A., Barreteau, H., Touze, T., Graille, M., Bouhss, A., Blanot, D., Van Tilbeurgh, H. & Mengin-Lecreulx, D. (2010). X-ray structure and site-directed mutagenesis analysis of the Escherichia coli colicin M immunity protein. Journal of Bacteriology 193, 205–214.CrossRefGoogle ScholarPubMed
Gerding, M. A., Ogata, Y., Pecora, N. D., Niki, H. & De Boer, P. A. (2007). The trans-envelope Tol–Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Molecular Microbiology 63, 1008–1025.CrossRefGoogle ScholarPubMed
Goemaere, E. L., Cascales, E. & Lloubes, R. (2007). Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. Journal of Molecular Biology 366, 1424–1436.CrossRefGoogle ScholarPubMed
Gokce, I., Raggett, E. M., Hong, Q., Virden, R., Cooper, A. & Lakey, J. H. (2000). The TolA-recognition site of colicin N. ITC, SPR and stopped-flow fluorescence define a crucial 27-residue segment. Journal of Molecular Biology 304, 621–632.CrossRefGoogle ScholarPubMed
Gorbalenya, A. E. (1994). Self-splicing group I and group II introns encode homologous (putative) DNA endonucleases of a new family. Protein Science 3, 1117–1120.CrossRefGoogle Scholar
Gorski, S. A., Capaldi, A. P., Kleanthous, C. & Radford, S. E. (2001). Acidic conditions stabilise intermediates populated during the folding of Im7 and Im9. Journal of Molecular Biology 312, 849–863.CrossRefGoogle ScholarPubMed
Gorski, S. A., Le Duff, C. S., Capaldi, A. P., Kalverda, A. P., Beddard, G. S., Moore, G. R. & Radford, S. E. (2004). Equilibrium hydrogen exchange reveals extensive hydrogen bonded secondary structure in the on-pathway intermediate of Im7. Journal of Molecular Biology 337, 183–193.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gsponer, J., Hopearuoho, H., Whittaker, S. B., Spence, G. R., Moore, G. R., Paci, E., Radford, S. E. & Vendruscolo, M. (2006). Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proceedings of the National Academy of Sciences, U. S. A. 103, 99–104.CrossRefGoogle ScholarPubMed
Hale, G. (2006). Therapeutic antibodies – delivering the promise? Advanced Drug Delivery Review 58(5–6), 633–639.CrossRefGoogle ScholarPubMed
Hands, S. L., Holland, L. E., Vankemmelbeke, M., Fraser, L., Macdonald, C. J., Moore, G. R., James, R. & Penfold, C. N. (2005). Interactions of TolB with the translocation domain of colicin E9 require an extended TolB box. Journal of Bacteriology 187, 6733–6741.CrossRefGoogle ScholarPubMed
Hecht, O., Ridley, H., Boetzel, R., Lewin, A., Cull, N., Chalton, D. A., Lakey, J. H. & Moore, G. R. (2008). Self-recognition by an intrinsically disordered protein. FEBS Letters 582, 2673–2677.CrossRefGoogle ScholarPubMed
Hecht, O., Ridley, H., Lakey, J. H. & Moore, G. R. (2009a). A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. Journal of Molecular Biology 388, 880–893.CrossRefGoogle ScholarPubMed
Hecht, O., Ridley, H., Lakey, J. H. & Moore, G. R. (2009b). A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. Journal of Molecular Biology 388, 880–893.CrossRefGoogle ScholarPubMed
Hecht, O., Zhang, Y., Li, C., Penfold, C. N., James, R. & Moore, G. R. (2010). Characterisation of the interaction of colicin A with its co-receptor TolA. FEBS Letters 584, 2249–2252.CrossRefGoogle ScholarPubMed
Herschman, H. R. & Helinski, D. R. (1967). Purification and characterization of colicin E2 and colicin E3. Journal of Biological Chemistry 242, 5360–5368.CrossRefGoogle ScholarPubMed
Hilsenbeck, J. L., Park, H., Chen, G., Youn, B., Postle, K. & Kang, C. (2004). Crystal structure of the cytotoxic bacterial protein colicin B at 2·5 A resolution. Molecular Microbiology 51, 711–720.CrossRefGoogle ScholarPubMed
Housden, N. G. & Kleanthous, C. (2011). Thermodynamic dissection of colicin interactions. Methods in Enzymology 488, 123–145.CrossRefGoogle ScholarPubMed
Housden, N. G., Loftus, S. R., Moore, G. R., James, R. & Kleanthous, C. (2005). Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proceedings of the National Academy of Sciences, U. S. A. 102, 13849–13854.CrossRefGoogle ScholarPubMed
Housden, N. G., Wojdyla, J. A., Korczynska, J., Grishkovskaya, I., Kirkpatrick, N., Brzozowski, A. M. & Kleanthous, C. (2010). Directed epitope delivery across the Escherichia coli outer membrane through the porin OmpF. Proceedings of the National Academy of Sciences, U.S.A 107, 21412–21417.CrossRefGoogle ScholarPubMed
Hsia, K. C., Chak, K. F., Liang, P. H., Cheng, Y. S., Ku, W. Y. & Yuan, H. S. (2004). DNA binding and degradation by the HNH protein ColE7. Structure 12, 205–214.CrossRefGoogle ScholarPubMed
Hullmann, J., Patzer, S. I., Romer, C., Hantke, K. & Braun, V. (2008). Periplasmic chaperone FkpA is essential for imported colicin M toxicity. Molecular Microbiology 69, 926–937.CrossRefGoogle ScholarPubMed
Iacovache, I., Van Der Goot, F. G. & Pernot, L. (2008). Pore formation: an ancient yet complex form of attack. Biochimica Biophysica Acta 1778(7–8), 1611–1623.CrossRefGoogle ScholarPubMed
Ito, K. & Akiyama, Y. (2005). Cellular functions, mechanism of action, and regulation of FtsH protease. Annual Review of Microbiology 59, 211–231.CrossRefGoogle ScholarPubMed
Jackson, S. E. (1998). How do small single-domain proteins fold? Fold Design 3, R81–91.CrossRefGoogle ScholarPubMed
Jakes, K. S., Davis, N. G. & Zinder, N. D. (1988). A hybrid toxin from bacteriophage f1 attachment protein and colicin E3 has altered cell receptor specificity. Journal of Bacteriology 170, 4231–4238.CrossRefGoogle ScholarPubMed
Jakes, K. S. & Finkelstein, A. (2010). The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Molecular Microbiology 75, 567–578.CrossRefGoogle ScholarPubMed
Joachimiak, L. A., Kortemme, T., Stoddard, B. L. & Baker, D. (2006). Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein–protein interface. Journal of Molecular Biology 361, 195–208.CrossRefGoogle Scholar
Johnson, A. E. & Van Waes, M. A. (1999). The translocon: a dynamic gateway at the ER membrane. Annual Review of Cell Development Biology 15, 799–842.CrossRefGoogle ScholarPubMed
Journet, L., Bouveret, E., Rigal, A., Lloubes, R., Lazdunski, C. & Benedetti, H. (2001). Import of colicins across the outer membrane of Escherichia coli involves multiple protein interactions in the periplasm. Molecular Microbiology 42, 331–344.CrossRefGoogle ScholarPubMed
Keeble, A. H., Joachimiak, L. A., Mate, M. J., Meenan, N., Kirkpatrick, N., Baker, D. & Kleanthous, C. (2008). Experimental and computational analyses of the energetic basis for dual recognition of immunity proteins by colicin endonucleases. Journal of Molecular Biology 379, 745–759.CrossRefGoogle ScholarPubMed
Keeble, A. H., Kirkpatrick, N., Shimizu, S. & Kleanthous, C. (2006). Calorimetric dissection of colicin DNase–immunity protein complex specificity. Biochemistry 45, 3243–3254.CrossRefGoogle ScholarPubMed
Keeble, A. H. & Kleanthous, C. (2005). The kinetic basis for dual recognition in colicin endonuclease-immunity protein complexes. Journal of Molecular Biology 352, 656–671.CrossRefGoogle ScholarPubMed
Keeble, A. H., Maté, M. J. & Kleanthous, C. (2005). HNH endonucleases. In Homing Endonucleases and Inteins, vol. 16 (eds. Belfort, M.Derbyshire, V.Stoddard, B. & Wood, D.), pp. 49–65. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Keenan, R. J., Freymann, D. M., Stroud, R. M. & Walter, P. (2001). The signal recognition particle. Annual Review of Biochemistry 70, 755–775.CrossRefGoogle ScholarPubMed
Khersonsky, O., Roodveldt, C. & Tawfik, D. S. (2006). Enzyme promiscuity: evolutionary and mechanistic aspects. Current Opinion in Chemical Biology 10, 498–508.CrossRefGoogle ScholarPubMed
Kiely, P. D. & Johnson, D. M. (2002). Infliximab and leflunomide combination therapy in rheumatoid arthritis: an open-label study. Rheumatology (Oxford) 41, 631–637.CrossRefGoogle ScholarPubMed
Kirkup, B. C. & Riley, M. A. (2004). Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428, 412.CrossRefGoogle ScholarPubMed
Kleanthous, C. (2010). Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nature Reviews Microbiology 8, 843–848.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kleanthous, C. & Walker, D. (2001). Immunity proteins: enzyme inhibitors that avoid the active site. Trends in Biochemical Sciences 26, 624–631.CrossRefGoogle ScholarPubMed
Knowling, S. E., Figueiredo, A. M., Whittaker, S. B., Moore, G. R. & Radford, S. E. (2009). Amino acid insertion reveals a necessary three-helical intermediate in the folding pathway of the colicin E7 immunity protein Im7. Journal of Molecular Biology 392, 1074–1086.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kortemme, T., Joachimiak, L. A., Bullock, A. N., Schuler, A. D., Stoddard, B. L. & Baker, D. (2004). Computational redesign of protein–protein interaction specificity. Nature Structural and Molecular Biology 11, 371–379.CrossRefGoogle ScholarPubMed
Krachler, A. M., Sharma, A., Cauldwell, A., Papadakos, G. & Kleanthous, C. (2010). TolA modulates the oligomeric status of YbgF in the bacterial periplasm. Journal of Molecular Biology 403, 270–285.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kuhlmann, U. C., Pommer, A. J., Moore, G. R., James, R. & Kleanthous, C. (2000). Specificity in protein–protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes. Journal of Molecular Biology 301, 1163.CrossRefGoogle ScholarPubMed
Kurisu, G., Zakharov, S. D., Zhalnina, M. V., Bano, S., Eroukova, V. Y., Rokitskaya, T. I., Antonenko, Y. N., Wiener, M. C. & Cramer, W. A. (2003). The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nature Structural Biology 10, 948–954.CrossRefGoogle ScholarPubMed
Lancaster, L. E., Savelsbergh, A., Kleanthous, C., Wintermeyer, W. & Rodnina, M. V. (2008). Colicin E3 cleavage of 16S rRNA impairs decoding and accelerates tRNA translocation on Escherichia coli ribosomes. Molecular Microbiology 69, 390–401.CrossRefGoogle ScholarPubMed
Lazzaroni, J. C., Dubuisson, J. F. & Vianney, A. (2002). The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins. Biochimie 84, 391–397.CrossRefGoogle Scholar
Le Duff, C. S., Whittaker, S. B., Radford, S. E. & Moore, G. R. (2006). Characterisation of the conformational properties of urea-unfolded Im7: implications for the early stages of protein folding. Journal of Molecular Biology 364, 824–835.CrossRefGoogle ScholarPubMed
Levin, K. B., Dym, O., Albeck, S., Magdassi, S., Keeble, A. H., Kleanthous, C. & Tawfik, D. S. (2009). Following evolutionary paths to protein–protein interactions with high affinity and selectivity. Nature Structural and Molecular Biology 16, 1049–1055.CrossRefGoogle ScholarPubMed
Li, W., Hamill, S. J., Hemmings, A. M., Moore, G. R., James, R. & Kleanthous, C. (1998). Dual recognition and the role of specificity-determining residues in colicin E9 DNase-immunity protein interactions. Biochemistry 37, 11771–11779.CrossRefGoogle ScholarPubMed
Li, W., Keeble, A. H., Giffard, C., James, R., Moore, G. R. & Kleanthous, C. (2004). Highly discriminating protein–protein interaction specificities in the context of a conserved binding energy hotspot. Journal of Molecular Biology 337, 743–759.CrossRefGoogle ScholarPubMed
Lin, Y. L., Elias, Y. & Huang, R. H. (2005). Structural and mutational studies of the catalytic domain of colicin E5: a tRNA-specific ribonuclease. Biochemistry 44, 10494–10500.CrossRefGoogle ScholarPubMed
Loftus, S. R., Walker, D., Mate, M. J., Bonsor, D. A., James, R., Moore, G. R. & Kleanthous, C. (2006). Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. Proceedings of the National Academy of Sciences, U. S. A. 103, 12353–12358.CrossRefGoogle ScholarPubMed
Lubkowski, J., Hennecke, F., Pluckthun, A. & Wlodawer, A. (1999). Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7, 711–722.CrossRefGoogle ScholarPubMed
Luna-Chavez, C., Lin, Y. L. & Huang, R. H. (2006). Molecular basis of inhibition of the ribonuclease activity in colicin E5 by its cognate immunity protein. Journal of Molecular Biology 358, 571–579.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Meenan, N. A., Sharma, A., Fleishman, S. J., Macdonald, C. J., Morel, B., Boetzel, R., Moore, G. R., Baker, D. & Kleanthous, C. (2010). The structural and energetic basis for high selectivity in a high-affinity protein–protein interaction. Proceedings of the National Academy of Sciences, U. S. A. 107, 10080–10085.CrossRefGoogle Scholar
Meng, G., Surana, N. K., St Geme, J. W. III & Waksman, G. (2006). Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO Journal 25, 2297–2304.CrossRefGoogle ScholarPubMed
Montalvao, R. W., Cavalli, A., Salvatella, X., Blundell, T. L. & Vendruscolo, M. (2008). Structure determination of protein–protein complexes using NMR chemical shifts: case of an endonuclease colicin-immunity protein complex. Journal of the American Chemical Society 130, 15990–15996.CrossRefGoogle ScholarPubMed
Mosbahi, K., Lemaitre, C., Keeble, A. H., Mobasheri, H., Morel, B., James, R., Moore, G. R., Lea, E. J. & Kleanthous, C. (2002). The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nature Structural Biology 9, 476–484.CrossRefGoogle ScholarPubMed
Mosbahi, K., Walker, D., James, R., Moore, G. R. & Kleanthous, C. (2006). Global structural rearrangement of the cell penetrating ribonuclease colicin E3 on interaction with phospholipid membranes. Protein Science 15, 620–627.CrossRefGoogle ScholarPubMed
Mosbahi, K., Walker, D., Lea, E., Moore, G. R., James, R. & Kleanthous, C. (2004). Destabilization of the colicin E9 Endonuclease domain by interaction with negatively charged phospholipids: implications for colicin translocation into bacteria. Journal of Biological Chemistry 279, 22145–22151.CrossRefGoogle ScholarPubMed
Ng, C. L., Lang, K., Meenan, N. A., Sharma, A., Kelley, A. C., Kleanthous, C. & Ramakrishnan, V. (2010a). Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nature Structural and Molecular Biology 17, 1241–1246.CrossRefGoogle ScholarPubMed
Ng, C. L., Lang, K., Meenan, N. A., Sharma, A., Kelley, A. C., Kleanthous, C. & Ramakrishnan, V. (2010b). Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nature Structural and Molecular Biology 17, 1241–1246.CrossRefGoogle ScholarPubMed
Nose, K. & Mizuno, D. (1968). Degradation of ribosomes in Escherichia coli cells treated with colicin E2. Journal of Biochemistry 64, 1–6.CrossRefGoogle ScholarPubMed
Ogawa, T., Inoue, S., Yajima, S., Hidaka, M. & Masaki, H. (2006). Sequence-specific recognition of colicin E5, a tRNA-targeting ribonuclease. Nucleic Acids Research 34, 6065–6073.CrossRefGoogle ScholarPubMed
Ogawa, T., Tomita, K., Ueda, T., Watanabe, K., Uozumi, T. & Masaki, H. (1999). A cytotoxic ribonuclease targeting specific transfer RNA anticodons. Science 283, 2097–2100.CrossRefGoogle ScholarPubMed
Oldham, R. K. & Dillman, R. O. (2008). Monoclonal antibodies in cancer therapy: 25 years of progress. Journal of Clinical Oncology 26, 1774–1777.CrossRefGoogle ScholarPubMed
Paci, E., Friel, C. T., Lindorff-Larsen, K., Radford, S. E., Karplus, M. & Vendruscolo, M. (2004). Comparison of the transition state ensembles for folding of Im7 and Im9 determined using all-atom molecular dynamics simulations with phi value restraints. Proteins 54, 513–525.CrossRefGoogle ScholarPubMed
Parsons, L. M., Lin, F. & Orban, J. (2006). Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45, 2122–2128.CrossRefGoogle Scholar
Penfold, C. N., Healy, B., Housden, N. G., Boetzel, R., Vankemmelbeke, M., Moore, G. R., Kleanthous, C. & James, R. (2004a). Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. Journal of Bacteriology 186, 4520–4527.CrossRefGoogle ScholarPubMed
Penfold, C. N., Healy, B., Housden, N. G., Boetzel, R., Vankemmelbeke, M., Moore, G. R., Kleanthous, C. & James, R. (2004b). Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. Journal of Bacteriology 186, 4520–4527.CrossRefGoogle ScholarPubMed
Pilsl, H. & Braun, V. (1998). The Ton system can functionally replace the TolB protein in the uptake of mutated colicin U. FEMS Microbiology Letters 164, 363–367.CrossRefGoogle ScholarPubMed
Pilsl, H., Smajs, D. & Braun, V. (1999). Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. Journal of Bacteriology 181, 3578–3581.CrossRefGoogle ScholarPubMed
Pohlschroder, M., Prinz, W. A., Hartmann, E. & Beckwith, J. (1997). Protein translocation in the three domains of life: variations on a theme. Cell 91, 563–566.CrossRefGoogle ScholarPubMed
Pokala, N. & Handel, T. M. (2001). Review: protein design – where we were, where we are, where we're going. Journal of Structural Biology 134, 269–281.CrossRefGoogle ScholarPubMed
Pommer, A. J., Cal, S., Keeble, A. H., Walker, D., Evans, S. J., Kuhlmann, U. C., Cooper, A., Connolly, B. A., Hemmings, A. M., Moore, G. R., James, R. & Kleanthous, C. (2001). Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9. Journal of Molecular Biology 314, 735.CrossRefGoogle ScholarPubMed
Postle, K. & Kadner, R. J. (2003). Touch and go: tying TonB to transport. Molecular Microbiology 49, 869–882.CrossRefGoogle ScholarPubMed
Pugh, S. D., Gell, C., Smith, D. A., Radford, S. E. & Brockwell, D. J. (2010). Single-molecule studies of the Im7 folding landscape. Journal of Molecular Biology 398, 132–145.CrossRefGoogle ScholarPubMed
Raggett, E. M., Bainbridge, G., Evans, L. J., Cooper, A. & Lakey, J. H. (1998). Discovery of critical Tol A-binding residues in the bactericidal toxin colicin N: a biophysical approach. Molecular Microbiology 28, 1335–1343.CrossRefGoogle ScholarPubMed
Ridley, H., Johnson, C. L. & Lakey, J. H. (2010). Interfacial interactions of pore-forming colicins. Advances in Experimental Medicine and Biology 677, 81–90.CrossRefGoogle ScholarPubMed
Riley, M. A. (1998). Molecular mechanisms of bacteriocin evolution. Annual Review of Genetics 32, 255–278.CrossRefGoogle ScholarPubMed
Roodveldt, C., Aharoni, A. & Tawfik, D. S. (2005). Directed evolution of proteins for heterologous expression and stability. Current Opinion in Structural Biology 15, 50–56.CrossRefGoogle ScholarPubMed
Senior, B. W. & Holland, I. B. (1971). Effect of colicin E3 upon the 30S ribosomal subunit of Escherichia coli. Proceedings of the National Academy of Sciencs, U. S. A. 68(5), 959–963.CrossRefGoogle ScholarPubMed
Sharma, O., Datsenko, K. A., Ess, S. C., Zhalnina, M. V., Wanner, B. L. & Cramer, W. A. (2009). Genome-wide screens: novel mechanisms in colicin import and cytotoxicity. Molecular Microbiology 73, 571–585.CrossRefGoogle ScholarPubMed
Sharma, O., Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Datsenko, K. A., Wanner, B. L. & Cramer, W. A. (2007). Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The outer membrane colicin translocon. Journal of Biological Chemistry 282, 23163–23170.CrossRefGoogle ScholarPubMed
Shi, Z., Chak, K. F. & Yuan, H. S. (2005). Identification of an essential cleavage site in ColE7 required for import and killing of cells. Journal of Biological Chemistry 280, 24663–24668.CrossRefGoogle ScholarPubMed
Shub, D. A., Goodrich-Blair, H. & Eddy, S. R. (1994). Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends in Biochemical Sciences 19, 402–404.CrossRefGoogle Scholar
Smallwood, C. R., Marco, A. G., Xiao, Q., Trinh, V., Newton, S. M. & Klebba, P. E. (2009). Fluoresceination of FepA during colicin B killing: effects of temperature, toxin and TonB. Molecular Microbiology 72, 1171–1180.CrossRefGoogle ScholarPubMed
Soelaiman, S., Jakes, K., Wu, N., Li, C. & Shoham, M. (2001). Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Molecular Cell 8, 1053–1062.CrossRefGoogle ScholarPubMed
Spector, J., Zakharov, S., Lill, Y., Sharma, O., Cramer, W. A. & Ritchie, K. (2010). Mobility of BtuB and OmpF in the Escherichia coli outer membrane: implications for dynamic formation of a translocon complex. Biophysical Journal 99, 3880–3886.CrossRefGoogle ScholarPubMed
Spence, G. R., Capaldi, A. P. & Radford, S. E. (2004). Trapping the on-pathway folding intermediate of Im7 at equilibrium. Journal of Molecular Biology 341, 215–226.CrossRefGoogle ScholarPubMed
Sutto, L., Latzer, J., Hegler, J. A., Ferreiro, D. U. & Wolynes, P. G. (2007). Consequences of localized frustration for the folding mechanism of the IM7 protein. Proceedings of the National Academy of Sciences, U. S. A. 104, 19825–19830.CrossRefGoogle ScholarPubMed
Tanford, C. (1970). Protein denaturation. C. Theoretical models for the mechanism of denaturation. Advanced Protein Chemistry 24, 1–95.CrossRefGoogle ScholarPubMed
Tokuriki, N. & Tawfik, D. S. (2009). Protein dynamism and evolvability. Science 324, 203–207.CrossRefGoogle ScholarPubMed
Tomita, K., Ogawa, T., Uozumi, T., Watanabe, K. & Masaki, H. (2000). A cytotoxic ribonuclease which specifically cleaves four isoaccepting arginine tRNAs at their anticodon loops. Proceedings of the National Academy of Sciences, U. S. A. 97, 8278–8283.CrossRefGoogle ScholarPubMed
Van Den Bremer, E. T., Keeble, A. H., Jiskoot, W., Spelbrink, R. E., Maier, C. S., Van Hoek, A., Visser, A. J., James, R., Moore, G. R., Kleanthous, C. & Heck, A. J. (2004). Distinct conformational stability and functional activity of four highly homologous endonuclease colicins. Protein Science 13, 1391–1401.CrossRefGoogle ScholarPubMed
Vankemmelbeke, M., Healy, B., Moore, G. R., Kleanthous, C., Penfold, C. N. & James, R. (2005). Rapid detection of colicin E9-induced DNA damage using Escherichia coli cells carrying SOS promoter–lux fusions. Journal of Bacteriology 187, 4900–4907.CrossRefGoogle ScholarPubMed
Vankemmelbeke, M., Zhang, Y., Moore, G. R., Kleanthous, C., Penfold, C. N. & James, R. (2009). Energy-dependent immunity protein release during tol-dependent nuclease colicin translocation. Journal of Biological Chemistry 284, 18932–18941.CrossRefGoogle ScholarPubMed
Vetter, I. R., Parker, M. W., Tucker, A. D., Lakey, J. H., Pattus, F. & Tsernoglou, D. (1998). Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6, 863–874.CrossRefGoogle Scholar
Walker, D., Lancaster, L., James, R. & Kleanthous, C. (2004a). Identification of the catalytic motif of the microbial ribosome inactivating cytotoxin colicin E3. Protein Science 13, 1603–1611.CrossRefGoogle ScholarPubMed
Walker, D., Moore, G. R., James, R. & Kleanthous, C. (2003). Thermodynamic consequences of bipartite immunity protein binding to the ribosomal ribonuclease colicin E3. Biochemistry 42, 4161.CrossRefGoogle Scholar
Walker, D., Mosbahi, K., Vankemmelbeke, M., James, R. & Kleanthous, C. (2007). The role of electrostatics in colicin nuclease domain translocation into bacterial cells. Journal of Biological Chemistry 282, 31389–31397.CrossRefGoogle ScholarPubMed
Walker, D., Rolfe, M., Thompson, A., Moore, G. R., James, R., Hinton, J. C. & Kleanthous, C. (2004b). Transcriptional profiling of colicin-induced cell death of Escherichia coli MG1655 identifies potential mechanisms by which bacteriocins promote bacterial diversity. Journal of Bacteriology 186, 866.CrossRefGoogle ScholarPubMed
Wallis, R., Leung, K. Y., Osborne, M. J., James, R., Moore, G. R. & Kleanthous, C. (1998). Specificity in protein–protein recognition: conserved Im9 residues are the major determinants of stability in the colicin E9 DNase–Im9 complex. Biochemistry 37, 476.CrossRefGoogle ScholarPubMed
Wallis, R., Moore, G. R., James, R. & Kleanthous, C. (1995). Protein–protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex. Biochemistry 34, 13743–13750.CrossRefGoogle ScholarPubMed
Wallis, R., Reilly, A., Barnes, K., Abell, C., Campbell, D. G., Moore, G. R., James, R. & Kleanthous, C. (1994). Tandem overproduction and characterisation of the nuclease domain of colicin E9 and its cognate inhibitor protein Im9. European Journal of Biochemistry 220, 447.CrossRefGoogle ScholarPubMed
Webster, R. E. (1991). The tol gene products and the import of macromolecules into Escherichia coli. Molecular Microbiology 5, 1005–1011.CrossRefGoogle ScholarPubMed
Whittaker, S. B., Spence, G. R., Gunter Grossmann, J., Radford, S. E. & Moore, G. R. (2007). NMR analysis of the conformational properties of the trapped on-pathway folding intermediate of the bacterial immunity protein Im7. Journal of Molecular Biology 366, 1001–1015.CrossRefGoogle ScholarPubMed
Wiener, M., Freymann, D., Ghosh, P. & Stroud, R. M. (1997). Crystal structure of colicin Ia. Nature 385, 461–464.CrossRefGoogle ScholarPubMed
Wiener, M. C. (2005). TonB-dependent outer membrane transport: going for Baroque? Current Opinion in Structural Biology 15, 394–400.CrossRefGoogle ScholarPubMed
Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Sharma, O. & Cramer, W. A. (2008). Crystal structures of the OmpF porin: function in a colicin translocon. EMBO Journal 27, 2171–2180.CrossRefGoogle Scholar
Zakharov, S. D. & Cramer, W. A. (2004). On the mechanism and pathway of colicin import across the E. Coli outer membrane. Frontiers in Bioscience 9, 1311–1317.CrossRefGoogle ScholarPubMed
Zakharov, S. D., Eroukova, V. Y., Rokitskaya, T. I., Zhalnina, M. V., Sharma, O., Loll, P. J., Zgurskaya, H. I., Antonenko, Y. N. & Cramer, W. A. (2004a). Colicin occlusion of OmpF and TolC channels: outer membrane translocons for colicin import. Biophysical Journal 87, 3901–3911.CrossRefGoogle ScholarPubMed
Zakharov, S. D., Kotova, E. A., Antonenko, Y. N. & Cramer, W. A. (2004b). On the role of lipid in colicin pore formation. Biochimica Biophysica Acta 1666, 239–249.CrossRefGoogle ScholarPubMed
Zakharov, S. D., Sharma, O., Zhalnina, M. V. & Cramer, W. A. (2008). Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF. Biochemistry 47, 12802–12809.CrossRefGoogle ScholarPubMed
Zakharov, S. D., Zhalnina, M. V., Sharma, O. & Cramer, W. A. (2006). The colicin E3 outer membrane translocon: immunity protein release allows interaction of the cytotoxic domain with OmpF porin. Biochemistry 45, 10199–10207.CrossRefGoogle ScholarPubMed
Zeth, K., Romer, C., Patzer, S. I. & Braun, V. (2008). Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. Journal of Biological Chemistry 283, 25324–25331.CrossRefGoogle ScholarPubMed
Zhang, X. Y., Goemaere, E. L., Seddiki, N., Celia, H., Gavioli, M., Cascales, E. & Lloubes, R. (2011). Mapping the interactions between Escherichia coli TolQ transmembrane segments. Journal of Biological Chemistry 286, 11756–11764.CrossRefGoogle ScholarPubMed
Zhang, X. Y., Goemaere, E. L., Thome, R., Gavioli, M., Cascales, E. & Lloubes, R. (2009a). Mapping the interactions between Escherichia coli tol subunits: rotation of the TolR transmembrane helix. Journal of Biological Chemistry 284, 4275–4282.CrossRefGoogle ScholarPubMed
Zhang, Y., Vankemmelbeke, M., Baardelang, P., Paoli, M., Penfold, C. N. & James, R. (2009b). The crystal structure of the TolB box of Colicin A in complex with TolB reveals important differences in the recruitment of the common TolB translocation portal used by group A colicins. Molecular Microbiology 75, 623–636.CrossRefGoogle Scholar
Zhang, Y., Vankemmelbeke, M. N., Holland, L. E., Walker, D. C., James, R. & Penfold, C. N. (2008). Investigating early events in receptor binding and translocation of colicin E9 using synchronized cell killing and proteolytic cleavage. Journal of Bacteriology 190, 4342–4350.CrossRefGoogle ScholarPubMed
Zhang, Y. L. & Cramer, W. A. (1992). Constraints imposed by protease accessibility on the trans-membrane and surface topography of the colicin E1 ion channel. Protein Science 1, 1666–1676.CrossRefGoogle ScholarPubMed