Outer membrane vesicle-mediated export of a pore-forming cytotoxin from Escherichia coli

Toxin Reviews

Volumn 25, Issue 1, 2006, Pages 31-46

  Kouokam, J Clavin ^a   Sun, Nyunt Wai ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

ClyA; Outer membrane vesicles; Pore forming toxin; Protein secretion

Indexed keywords

CHOLESTEROL; CYTOLYSIN; CYTOLYSIN A; CYTOTOXIN; OLIGOMER; SIGNAL PEPTIDE; TYPHOID VACCINE; UNCLASSIFIED DRUG;

BACTERIAL MEMBRANE; ELECTRON MICROSCOPY; ENTEROBACTERIACEAE; ESCHERICHIA COLI; HUMAN; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE VESICLE; NONHUMAN; OUTER MEMBRANE; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI;

EID: 32844455630     PISSN: 15569543     EISSN: 15569551     Source Type: Journal    
DOI: 10.1080/15569540500320888     Document Type: Review

References (56)

1. Atkins, A., Wyborn, N. R., Wallace, A. J., Stillman, T. J., Black, L. K., Fielding, A. B., Hisakado, M., Artymiuk, P. J., Green, J. (2000). Structure-function relationships of a novel bacterial toxin, hemolysin E. The role of alpha G. J. Biol. Chem. 275(52):41150-41155.
2. Ballard, J., Crabtree, J., Roe, B. A., Tweten, R. K. (1995). The primary structure of Clostridium septicum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infect. Immun. 63(1):340-344.
3. Benz, R., Janko, K., Boos, W., Lauger, P. (1978). Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli. Biochim. Biophys. Acta 511(3):305-319.
4. Beveridge, T. J. (1999). Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725-4733.
5. Bhakdi, S., Bayley, H., Valeva, A., Walev, I., Walker, B., Kehoe, M., Palmer, M. (1996a). Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165(2):73-79.
6. Bhakdi, S., Walev, I., Jonas, D., Palmer, M., Weller, U., Suttorp, N., Grimminger, F., Seeger, W. (1996b). Pathogenesis of sepsis syndrome: possible relevance of pore-forming bacterial toxins. Curr. Top. Microbiol. Immunol. 216:101-118.
7. Christie, P. J. (2001). Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
8. Christie, P. J., Vogel, J. P. (2000). Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
9. del Castillo, F. J., Leal, S. C., Moreno, F., del Castillo, I. (1997). The Escherichia coli K-12 sheA gene encodes a 34-kDa secreted haemolysin. Mol. Microbiol. 25(1):107-115.
10. del Castillo, F. J., Moreno, F., del Castillo, I. (2001). Secretion of the Escherichia coli K-12 SheA hemolysin is independent of its cytolytic activity. FEMS Microbiol. Lett. 204(2):281-285.
11. Dhople, V. M., Nagaraj, R. (1995). Generation of analogs having potent antimicrobial and hemolytic activities with minimal changes from an inactive 16-residue peptide corresponding to the helical region of Staphylococcus aureus delta-toxin. Protein Eng. 8(3):315-318.
12. Fiocca, R., Necchi, V., Sommi, P., Ricci, V., Telford, J., Cover, T. L., Solcia, E. (1999). Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 188:220-226.
13. Galan, J. E., Collmer, A. (1999). Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
14. Galen, J. E., Zhao, L., Chinchilla, M., Wang, J. Y., Pasetti, M. F., Green, J., Levine, M. M. (2004). Adaptation of the endogenous Salmonella enterica serovar Typhi clyA-encoded hemolysin for antigen export enhances the immunogenicity of anthrax protective antigen domain 4 expressed by the attenuated live-vector vaccine strain CVD 908-htrA. Infect. Immun. 72(12):7096-7106.
15. Green, J., Baldwin, M. L. (1997). The molecular basis for the differential regulation of the hlyE-encoded haemolysin of Escherichia coli by FNR and HlyX lies in the improved activating region 1 contact of HlyX. Microbiology 143(12):3785-3793.
16. Grindley, H. M., Artymiuk, P. J., Rice, D. W., Willett, P. (1993). Identification of tertiary structure resemblance in proteins using a maximal common subgraph isomorphism algorithm. J. Mol. Biol. 229(3):707-721.
17. Hacker, J., Hughes, C., Hof, H., Goebel, W. (1983). Cloned hemolysin genes from Escherichia coli that cause urinary tract infection determine different levels of toxicity in mice. Infect. Immun. 42(1):57-63.
18. Harris, N. L., Presnell, S. R., Cohen, F. E. (1994). Four helix bundle diversity in globular proteins. J. Mol. Biol. 236(5):1356-1368.
19. Henderson, I. R., Cappello, R., Nataro, J. P. (2000). Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8:534-535.
20. Horstman, A. L., Kuehn, M. J. (2000). Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 275(17):12489-12496.
21. Hueck, C. J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
22. Kadurugamuwa, J. L., Beveridge, T. J. (1998). Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles. Antimicrob. Agents Chemother. 42:1476-1483.
23. Kadurugamuwa, J. L., Beveridge, T. J. (1999). Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other gram-negative bacteria. Microbiology 145(8):2051-2060.
24. Kato, S., Kowashi, Y., Demuth, D. R. (2002). Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb. Pathog. 32, 1-13.
25. Koronakis, V., Hughes, C. (1993). Bacterial signal peptide-independent protein export: HlyB-directed secretion of hemolysin. Semin. Cell Biol. 4:7-15.
26. Koronakis, V., Hughes, C., Koronakis, E. (1991). Energetically distinct early and late stages of HlyB/HlyD-dependent secretion across both Escherichia coli membranes. Embo J. 10:3263-3272.
27. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., Hughes, C. (2000). Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914-919.
28. Koster, M., Bitter, W., Tommassen, J. (2000). Protein secretion mechanisms in Gram-negative bacteria. Int. J. Med. Microbiol 290:325-331.
29. Lai, X. H., Arencibia, L, Johansson, A., Wai, S. N., Oscarsson, J., Kalfas, S., Sundqvist, K. G., Mizunoe, Y., Sjostedt, A., Uhlin, B. E. (2000). Cytocidal and apoptotic effects of the ClyA protein from Escherichia coli on primary and cultured monocytes and macrophages. Infect. Immun. 68(7):4363-4367.
30. Ludwig, A., Tengel, C., Bauer, S., Bubert, A., Benz, R., Mollenkopf, H. J., Goebel, W. (1995). Sly A, a regulatory protein from Salmonella, typhimurium, induces a haemolytic and pore-forming protein in Escherichia coli. Mol. Gen. Genet. 249(5):474-486.
31. Ludwig, A., Bauer, S., Benz, R., Bergmann, B., Goebel, W. (1999). Analysis of the SlyA-controlled expression, subcellular localization and pore-forming activity of a 34 kDa haemolysin (ClyA) from Escherichia coli K-12. Mol. Microbiol. 31(2):557-567.
32. Ludwig, A., von Rhein, C., Bauer, S., Huttinger, C., Goebel, W. (2004). Molecular analysis of cytolysin A (ClyA) in pathogenic Escherichia coli strains. J. Bacteriol. 186(16):5311-5320.
33. Oscarsson, J., Mizunoe, Y., Uhlin, B. E., Haydon, D. J. (1996). Induction of haemolytic activity in Escherichia coli by the slyA gene product. Mol. Microbiol. 20(1):191-199.
34. Oscarsson, J., Mizunoe, Y., Li, L., Lai, X. H., Wieslander, A., Uhlin, B. E. (1999). Molecular analysis of the cytolytic protein ClyA (SheA) from Escherichia coli. Mol. Microbiol. 32(6):1226-1238.
35. Oscarsson, J., Westermark, M., Lofdahl, S., Olsen, B., Palmgren, H., Mizunoe, Y., Wai S. N., Uhlin, B. E. (2002). Characterization of a pore-forming cytotoxin expressed by Salmonella, enterica serovars typhi and paratyphi A. Infect. Immun. 70(10):5759-5769.
36. Parkhill, J., Dougan, G., James, K. D., Thomson, N. R., Pickard, D., Wain, J., Churcher, C., Mungall, K. L., Bentley, S. D., Holden, M. T. and others. (2001). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413(6858):848-852.
37. Pugsley, A. P. (1993). The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
38. Sandkvist, M. (2001a). Biology of type II secretion. Mol. Microbiol. 40:71-283.
39. Sandkvist, M. (2001b). Type II secretion and pathogenesis. Infect. Immun. 69:3523-3535.
40. Sargent, F., Bogsch, E. G., Stanley, N. R., Wexler, M., Robinson, C., Berks, B. C., Palmer, T. (1998). Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17:3640-3650.
41. 2+ signalling and Toll-like receptor 4. Cellular Microbiology Online Early.
42. Spory, A., Bosserhoff, A., von Rhein, C., Goebel, W., Ludwig, A. (2002). Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. J. Bacteriol. 184(13):3549-3559.
43. Stanley, P., Packman, L. C., Koronakis, V., Hughes, C. (1994). Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266(5193):1992-1996.
44. 2+ oscillations in renal epithelial cells. Nature 405(6787):694-697.
45. Uhlich, G. A., McNamara, P. J., landolo, J. J., Mosier, D. A. (1999). Cloning and characterization of the gene encoding Pasteurella haemolytica FnrP, a regulator of the Escherichia coli silent hemolysin sheA. J. Bacteriol. 181(12):3845-3848.
46. Vallance, B. A., Finlay, B. B. (2000). Exploitation of host cells by enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 97:8799-8806.
47. Wai, S. N., Takade, A., Amako, K. (1995). The release of outer membrane vesicles from the strains of enterotoxigenic Escherichia coli. Microbiol. Immunol. 39(7):451-456.
48. Wai, S. N., Lindmark, B., Soderblom, T., Takade, A., Westermark, M., Oscarsson, J., Jass, J., Richter-Dahlfors, A., Mizunoe, Y., Uhlin, B. E. (2003a). Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115(1):25-35.
49. Wai, S. N., Westermark, M., Oscarsson, J., Jass, J., Maier, E., Benz, R., Uhlin, B. E. (2003b). Characterization of dominantly negative mutant ClyA cytotoxin proteins in Escherichia coli. J. Bacteriol. 185(18):5491-5499.
50. Walev, I., Vollmer, P., Palmer, M., Bhakdi, S., Rose-John, S. (1996). Pore-forming toxins trigger shedding of receptors for interleukin 6 and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 93(15):7882-7887.
51. Wallace, A. J., Stillman, T. J., Atkins, A., Jamieson, S. J., Bullough, P. A., Green, J., Artymiuk, P.J. (2000). E. coli hemolysin E (HlyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy. Cell 100(2):265-276.
52. Walton, J. R., Smith, D. H. (1969). New hemolysin (gamma) produced by Escherichia coli. J. Bacteriol. 98(1):304-305.
53. Welch, R. A., Dellinger, E. P., Minshew, B., Falkow, S. (1981). Haemolysin contributes to virulence of extra-intestinal E. coli infections. Nature 294(5842):665-667.
54. Westermark, M., Oscarsson, J., Mizunoe, Y., Urbonaviciene, J., Uhlin, B. E. (2000). Silencing and activation of ClyA cytotoxin expression in Escherichia coli. J. Bacteriol. 182(22):6347-6357.
55. Wyborn, N. R., Clark, A., Roberts, R. E., Jamieson, S. J., Tzokov, S., Bullough, P. A., Stillman, T. J., Artymiuk, P. J., Galen, J. E., Zhao, L. and others. (2004). Properties of haemolysin E (HlyE) from a pathogenic Escherichia coli avian isolate and studies of HlyE export. Microbiology 150(5):1495-1505.
56. Yadav, S. P., Kundu, B., Ghosh, J. K. (2003). Identification and characterization of an amphipathic leucine zipper-like motif in Escherichia coli toxin hemolysin E. Plausible role in the assembly and membrane destabilization. J. Biol. Chem. 278(51):51023-51034.