Swimming against the tide: Progress and challenges in our understanding of colicin translocation

Nature Reviews Microbiology

Volumn 8, Issue 12, 2010, Pages 843-848

  Kleanthous, Colin ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLICIN;

BACTERIAL CELL; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TRANSLOCATION LINE; YERSINIA PESTIS;

CELL MEMBRANE; COLICINS; ESCHERICHIA COLI; PROTEIN TRANSPORT;

ESCHERICHIA COLI;

EID: 78449293752     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2454     Document Type: Review

References (56)

1. Riley M. A. & Wertz, J. E. Bacteriocins: evolution, ecology and application. Annu. Rev. Microbiol. 56 117-137 (2002).
2. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan,B. J. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418, 171-174 (2002).
3. Kirkup, B. C. & Riley, M. A. Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 428, 412 (2004).
4. Majeed, H., Gillor, O., Kerr, B. & Riley, M. A. Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J. 22 Jul 2010 (doi:10.1038/ismej.2010.90).
5. Gillor, O., Etzion, A. & Riley, M. A. The dual role of bacteriocins as anti-and probiotics. Appl. Microbiol. Biotechnol. 81, 591-606 (2008).
6. Gordon, D. M. The potential of bacteriocin-producing probiotics and associated caveats. Future Microbiol.4, 941-943 (2008).
7. Schamberger, G. P., Phillips, R. L., Jacobs, J. L. &Diez-Gonzalez, F. Reduction of Escherichia coliO157:H7 populations in cattle by addition of colicinE7-producing E. coli to feed. Appl. Environ. Microbiol.70, 6053-6060 (2004).
8. Gratia, A. Sur un remarquable exemple d'antagonisme entre deux souches de colibacille. C. R. Soc. Biol. 93, 1040-1041 (1925) (in French).
9. Cascales, E. et al. Colicin biology. Microbiol. Mol. Biol. R e v. 71, 158-229 (2007).
10. Wiener, M., Freymann, D., Ghosh, P. & Stroud, R. M. Crystal structure of colicin Ia. Nature 385, 461-464 (1997).
11. Soelaiman, S., Jakes, K., Wu, N., Li, C. & Shoham, M. Crystal structure of colicin E3: implications for cell entry and ribosome inactivation. Mol. Cell 8, 1053-1062 (2001).
12. Hilsenbeck, J. L. et al. Crystal structure of the cytotoxic bacterial protein colicin B at 2.5 Å resolution. Mol. Microbiol. 51, 711-720 (2004).
13. Vetter, I. R. et al. Crystal structure of a colicin N-fragment suggests a model for toxicity. Structure 6, 863-874 (1998).
14. Zeth, K., Romer, C., Patzer, S. I. & Braun, V. Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. J. Biol. Chem. 283, 25324-25331 (2008).
15. Arnold, T., Zeth, K. & Linke, D. Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J. Biol. Chem. 284, 6403-6413 (2009).
16. Anderluh, G., Gokce, I. & Lakey, J. H. A natively unfolded toxin domain uses its receptor as a folding template. J. Biol. Chem. 279, 22002-22009 (2004).
17. Collins, E. S. et al. Structural dynamics of the membrane translocation domain of colicin E9 and its interaction with TolB. J. Mol. Biol. 318, 787-804 (2002).
18. Schaller, K. & Nomura, M. Colicin E2 is DNA endonuclease. Proc. Natl Acad. Sci. USA 73, 3989-3993 (1976).
19. Jakes, K. S. & Zinder, N. D. Highly purified colicin E3 contains immunity protein. Proc. Natl Acad. Sci. USA71, 3380-3384 (1974).
20. Olschläger, T., Turba, A. & Braun, V. Binding of theimmunity protein inactivates colicin M. Mol. Microbiol.5, 1105-1111 (1991).
21. Kleanthous, C. & Walker, D. Immunity proteins: enzyme inhibitors that avoid the active site. Trends Biochem. Sci. 26, 624-631 (2001).
22. Gillor, O., Vriezen, J. A. & Riley, M. A. The role of SOS boxes in enteric bacteriocin regulation. Microbiology 154, 1783-1792 (2008).
23. 12 and theE colicins on the outer membrane of the cell envelope. J. Bacteriol. 11 5, 506-513 (1973).
24. Kurisu, G. et al. The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nature Struct. Biol. 10, 948-954 (2003).
25. Sharma, O. et al. Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The membrane colicin translocon. J. Biol. Chem. 282, 23163-23170 (2007).
26. Buchanan, S. K. et al. Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J. 26, 2594-2604 (2007).
27. Housden, N. G., Loftus, S. R., Moore, G. R., James, R. & Kleanthous, C. Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proc. Natl Acad. Sci. USA 102, 13849-13854 (2005).
28. Jakes, K. & Finkelstein, A. The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol. Microbiol. 75, 567-578 (2009).
29. Zakharov, S. D., Sharma, O., Zhalnina, M. V. & Cramer, W. A. Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF. Biochemistry 47, 12802-12809 (2008).
30. Zakharov, S. D. et al. Colicin occlusion of OmpF and TolC channels: outer membrane translocons for colicin import. Biophys. J. 87, 3901-3911 (2004).
31. Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Sharma, O. & Cramer, W. A. Crystal structures of the OmpF porin: function in a colicin translocon. EMBO J. 27, 2171-2180 (2008).
32. Baboolal, T. G. et al. Colicin N binds to the periphery of its receptor and translocator, outer membrane protein F. Structure 16, 371-379 (2008).
33. Anderluh, G. et al. Concerted folding and binding of a flexible colicin domain to its periplasmic receptor TolA. J. Biol. Chem. 278, 21860-21868 (2003).
34. Bonsor, D. A. et al. Allosteric β-propeller signalling in TolB and its manipulation by translocating colicins. EMBO J. 28, 2846-2857 (2009).
35. Zhang, Y. et al. 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. Mol. Microbiol. 75, 623-636 (2009).
36. Cadieux, N., Phan, P. G., Cafiso, D. S. & Kadner, R. J. Differential substrate-induced signaling through the TonB-dependent transporter BtuB. Proc. Natl Acad. Sci. USA 100, 10688-10693 (2003).
37. Wiener, M. C. TonB-dependent outer membrane transport: going for Baroque? Curr. Opin. Struct. Biol. 15, 394-400 (2005).
38. Kleanthous, C. Translocator hunt comes full Cir-Col. Mol. Microbiol. 75, 529-533 (2009).
39. Pilsl, H. & Braun, V. The To n system can functionally replace the TolB protein in the uptake of mutated colicin U. FEMS Microbiol. Lett. 164, 363-367 (1998).
40. de Zamaroczy, M., Mora, L., Lecuyer, A., Geli, V. & Buckingham, R. H. Cleavage of colicin D is necessary for cell killing and requires the inner membrane peptidase LepB. Mol. Cell 8, 159-168 (2001).
41. Shi, Z., Chak, K. F. & Yuan, H. S. Identification of an essential cleavage site in ColE7 required for import and killing of cells. J. Biol. Chem. 280, 24663-24668 (2005).
42. Walker, D., Mosbahi, K., Vankemmelbeke, M., James, R. & Kleanthous, C. The role of electrostatics in colicin nuclease domain translocation into bacterial cells.J. Biol. Chem. 282, 31389-31397 (2007).
43. Mosbahi, K. et al. The cytotoxic domain of colicin E9 is a channel-forming endonuclease. Nature Struct. Biol. 9, 476-484 (2002).
44. Mosbahi, K., Walker, D., James, R., Moore, G. R. & Kleanthous, C. Global structural rearrangement of the cell penetrating ribonuclease colicin E3 on interaction with phospholipid membranes. Protein Sci. 15, 620-627 (2006).
45. Benedetti, H., Lloubes, R., Lazdunski, C. & Letellier, L. Colicin A unfolds during its translocation in Escherichia coli cells and spans the whole cell envelope when its pore has formed. EMBO J. 11, 441-447 (1992).
46. Duche, D. Colicin E2 is still in contact with its receptor and import machinery when its nuclease domain enters the cytoplasm. J. Bacteriol. 189, 4217-4222 (2007).
47. Cascales, E., Gavioli, M., Sturgis, J. N. & Lloubes, R. Proton motive force drives the interaction of the inner membrane TolA and outer membrane Pal proteins in Escherichia coli. Mol. Microbiol. 38, 904-915 (2000).
48. Gerding, M. A., Ogata, Y., Pecora, N. D., Niki, H. & de Boer, P. A. 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. Mol. Microbiol. 63, 1008-1025 (2007).
49. Bonsor, D. A., Grishkovskaya, I., Dodson, E. J. & Kleanthous, C. Molecular mimicry enables competitive recruitment by a natively disordered protein. J. Am. Chem. Soc. 15, 4800-4807 (2007).
50. Loftus, S. R. et al. Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. Proc. Natl Acad. Sci. USA 103, 12353-12358 (2006).
51. Vankemmelbeke, M. N. et al. Energy dependent immunity protein release during tol-dependent nuclease colicin translocation. J. Biol. Chem. 284, 18932-18941 (2009).
52. Witty, M. et al. Structure of the periplasmic domain of Pseudomonas aeruginosa TolA: evidence for an evolutionary relationship with the TonB transporter protein. EMBO J. 21, 4207-4218 (2002).
53. Noinaj, N., Guillier, M., Barnard, T. J. & Buchanan, S. K. TonB-dependent transporters: regulation, structure and function. Annu. Rev. Microbiol. 64, 43-60 (2010).
54. Hecht, O., Ridley, H., Lakey, J. H. & Moore, G. R.A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. J. Mol. Biol. 388, 880-893 (2009).
55. Jakes, K. S., Davis, N. G. & Zinder, N. D. A hybridtoxin from bacteriophage f1 attachment protein andcolicin E3 has altered cell receptor specificity.J. Bacteriol. 170, 4231-4238 (1988).
56. Braun, V. & Herrmann, C. Evolutionary relationship ofuptake systems for biopolymers in Escherichia coli:cross-complementation between the TonB-ExbB-ExbDand the TolA-TolA-TolR proteins. Mol. Microbiol. 8,261-268 (1993).