Release of the type I secreted α-haemolysin via outer membrane vesicles from Escherichia coli

Molecular Microbiology

Volumn 59, Issue 1, 2006, Pages 99-112

  Balsalobre, Carlos ^a,c   Silván, Jose Manuel ^a   Berglund, Stina ^a   Mizunoe, Yoshimitsu ^b   Uhlin, Bernt Eric ^a   Wai, Sun Nyunt ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYSIN; PROTEINASE; TOLC PROTEIN;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOLYSIS; ERYTHROCYTE; ESCHERICHIA COLI; HOST CELL; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; CYTOPLASMIC VESICLES; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FATTY ACIDS; HELA CELLS; HEMOLYSIN PROTEINS; HUMANS; MEMBRANE TRANSPORT PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33645070224     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04938.x     Document Type: Article

References (51)

1. Balsalobre C. Juarez A. Madrid C. Mourino M. Prenafeta A. Munoa FJ. 1996 Complementation of the hha mutation in Escherichia coli by the ymoA gene from Yersinia enterocolitica: dependence on the gene dosage Microbiology 142 Part 7 1841 1846
2. Bauer ME. Welch RA. 1996 Association of RTX toxins with erythrocytes Infect Immun 64 4665 4672
3. Bauer ME. Welch RA. 1997 Pleiotropic effects of a mutation in rfaC on Escherichia coli hemolysin Infect Immun 65 2218 2224
4. Beveridge TJ. 1999 Structures of Gram-negative cell walls and their derived membrane vesicles J Bacteriol 181 4725 4733
5. Bolivar F. Rodriguez RL. Greene PJ. Betlach MC. Heyneker HL. Boyer HW. 1977 Construction and characterization of new cloning vehicles. II. A multipurpose cloning system Gene 2 95 113
6. Carter P. Bedouelle H. Winter G. 1985 Improved oligonucleotide site-directed mutagenesis using M13 vectors Nucleic Acids Res 13 4431 4443
7. Casadaban MJ. Cohen SN. 1980 Analysis of gene control signals by DNA fusion and cloning in Escherichia coli J Mol Biol 138 179 207
8. Chang AC. Cohen SN. 1978 Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid J Bacteriol 134 1141 1156
9. Cheng LW. Schneewind O. 2000 Yersinia enterocolitica TyeA, an intracellular regulator of the type III machinery, is required for specific targeting of YopE, YopH, YopM, and YopN into the cytosol of eukaryotic cells J Bacteriol 182 3183 3190
10. Demuth DR. James D. Kowashi Y. Kato S. 2003 Interaction of Actinobacillus actinomycetemcomitans outer membrane vesicles with HL60 cells does not require leukotoxin Cell Microbiol 5 111 121
11. Felmlee T. Welch RA. 1988 Alterations of amino acid repeats in the Escherichia coli hemolysin affect cytolytic activity and secretion Proc Natl Acad Sci USA 85 5269 5273
12. Fernandez LA. de Lorenzo V. 2001 Formation of disulphide bonds during secretion of proteins through the periplasmic-independent type I pathway Mol Microbiol 40 332 346
13. Fernandez LA. Sola I. Enjuanes L. de Lorenzo V. 2000 Specific secretion of active single-chain Fv antibodies into the supernatants of Escherichia coli cultures by use of the hemolysin system Appl Environ Microbiol 66 5024 5029
14. Godessart N. Munoa FJ. Regue M. Juarez A. 1988 Chromosomal mutations that increase the production of a plasmid-encoded haemolysin in Escherichia coli J Gen Microbiol 134 2779 2787
15. 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 57 63
16. Henning U. Schwarz H. Chen R. 1979 Radioimmunological screening method for specific membrane proteins Anal Biochem 97 153 157
17. Horstman AL. Kuehn MJ. 2000 Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles J Biol Chem 275 12489 12496
18. Horstman AL. Kuehn MJ. 2002 Bacterial surface association of heat-labile enterotoxin through lipopolysaccharide after secretion via the general secretory pathway J Biol Chem 277 32538 32545
19. Hull SI. Hull RA. Minshew BH. Falkow S. 1982 Genetics of hemolysin of Escherichia coli J Bacteriol 151 1006 1012
20. Jensen KF. 1993 The Escherichia coli K-12 'wild types' W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels J Bacteriol 175 3401 3407
21. Johansson J. Balsalobre C. Wang SY. Urbonaviciene J. Jin DJ. Sonden B. Uhlin BE. 2000 Nucleoid proteins stimulate stringently controlled bacterial promoters: a link between the cAMP-CRP and the (p)ppGpp regulons in Escherichia coli Cell 102 475 485
22. Kadurugamuwa JL. Beveridge TJ. 1995 Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion J Bacteriol 177 3998 4008
23. Kato S. Kowashi Y. Demuth DR. 2002 Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin Microb Pathog 32 1 13
24. Kesty NC. Mason KM. Reedy M. Miller SE. Kuehn MJ. 2004 Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells EMBO J 23 4538 4549
25. Kolling GL. Matthews KR. 1999 Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7 Appl Environ Microbiol 65 1843 1848
26. Koronakis V. 2003 TolC - the bacterial exit duct for proteins and drugs FEBS Lett 555 66 71
27. Laemmli, U.K. 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685
28. Lai XH. Wang SY. Uhlin BE. 1999 Expression of cytotoxicity by potential pathogens in the standard Escherichia coli collection of reference (ECOR) strains Microbiology 145 3295 3303
29. Lally ET. Hill RB. Kieba IR. Korostoff J. 1999 The interaction between RTX toxins and target cells Trends Microbiol 7 356 361
30. Ludwig A. Vogel M. Goebel W. 1987 Mutations affecting activity and transport of haemolysin in Escherichia coli Mol Gen Genet 206 238 245
31. Moayeri M. Welch RA. 1997 Prelytic and lytic conformations of erythrocyte-associated Escherichia coli hemolysin Infect Immun 65 2233 2239
32. Mourino M. Munoa F. Balsalobre C. Diaz P. Madrid C. Juarez A. 1994 Environmental regulation of alpha-haemolysin expression in Escherichia coli Microb Pathog 16 249 259
33. Nicaud JM. Mackman N. Gray L. Holland IB. 1986 The C-terminal, 23 kDa peptide of E. coli haemolysin 2001 contains all the information necessary for its secretion by the haemolysin (Hly) export machinery FEBS Lett 204 331 335
34. Ochman H. Selander RK. 1984 Standard reference strains of Escherichia coli from natural populations J Bacteriol 157 690 693
35. Oropeza-Wekerle RL. Muller E. Kern P. Meyermann R. Goebel W. 1989 Synthesis, inactivation, and localization of extracellular and intracellular Escherichia coli hemolysins J Bacteriol 171 2783 2788
36. Oscarsson J. Mizunoe Y. Li L. Lai XH. Wieslander A. Uhlin BE. 1999 Molecular analysis of the cytolytic protein ClyA (SheA) from Escherichia coli Mol Microbiol 32 1226 1238
37. Pellett S. Boehm DF. Snyder IS. Rowe G. Welch RA. 1990 Characterization of monoclonal antibodies against the Escherichia coli hemolysin Infect Immun 58 822 827
38. Saunders NB. Shoemaker DR. Brandt BL. Moran EE. Larsen T. Zollinger WD. 1999 Immunogenicity of intranasally administered meningococcal native outer membrane vesicles in mice Infect Immun 67 113 119
39. Shoberg RJ. Thomas DD. 1993 Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture Infect Immun 61 3892 3900
40. Stanley PL. Diaz P. Bailey MJ. Gygi D. Juarez A. Hughes C. 1993 Loss of activity in the secreted form of Escherichia coli haemolysin caused by an rfaP lesion in core lipopolysaccharide assembly Mol Microbiol 10 781 787
41. Stanley P. Koronakis V. Hughes C. 1998 Acylation of Escherichia coli hemolysin: a unique protein lipidation mechanism underlying toxin function Microbiol Mol Biol Rev 62 309 333
42. Thanabalu T. Koronakis E. Hughes C. Koronakis V. 1998 Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore EMBO J 17 6487 6496
43. Towbin H. Staehelin T. Gordon J. 1979 Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications Proc Natl Acad Sci USA 76 4350 4354
44. Tzschaschel BD. Guzman CA. Timmis KN. de Lorenzo V. 1996 An Escherichia coli hemolysin transport system-based vector for the export of polypeptides: export of Shiga-like toxin IIeB subunit by Salmonella typhimurium aroA Nat Biotechnol 14 765 769
45. Wai SN. Takade A. Amako K. 1995 The release of outer membrane vesicles from the strains of enterotoxigenic Escherichia coli Microbiol Immunol 39 451 456
46. Wai SN. Mizunoe Y. Takade A. Kawabata SI. Yoshida SI. 1998 Vibrio cholerae O1 strain TSI-4 produces exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation Appl Environ Microbiol 64 3648 3655
47. Wai SN. Lindmark B. Soderblom T. Takade A. Westermark M. Oscarsson J. et al. 2003 Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin Cell 115 25 35
48. Wandersman C. Delepelaire P. 1990 TolC, an Escherichia coli outer membrane protein required for hemolysin secretion Proc Natl Acad Sci USA 87 4776 4780
49. Wandersman C. Letoffe S. 1993 Involvement of lipopolysaccharide in the secretion of Escherichia coli alpha-haemolysin and Erwinia chrysanthemi proteases Mol Microbiol 7 141 150
50. Welch RA. 1991 Pore-forming cytolysins of Gram-negative bacteria Mol Microbiol 5 521 528
51. Welch RA. Dellinger EP. Minshew B. Falkow S. 1981 Haemolysin contributes to virulence of extra-intestinal E. coli infections Nature 294 665 667