Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions

Journal of Bacteriology

Volumn 181, Issue 22, 1999, Pages 7014-7020

  Maurer, Jochen ^a,c   Jose, Joachim ^a,d   Meyer, Thomas F ^a,b  

^a MAX PLANCK INST FÜR BIOLOGIE   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c Creatogen Live Vaccines GmbH   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AMINO ACID; CHOLERA TOXIN; HYBRID PROTEIN; PROTEIN;

ARTICLE; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; ELECTROPHORETIC MOBILITY; ESCHERICHIA COLI; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0032698497     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.22.7014-7020.1999     Document Type: Article

References (54)

1. Anderson, D. M., and O. Schneewind. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-1143.
2. Baneyx, F., A. Ayling, T. Palumbo, D. Thomas, and G. Georgiou. 1991. Optimization of growth conditions for the production of proteolytically-sensitive proteins in the periplasmic space of Escherichia coli, Appl. Microbiol. Biotechnol. 36:14-20.
3. Baneyx, F., and G. Georgiou. 1990. In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172:491-494.
4. Baneyx, F., and G. Georgiou. 1991. Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecular-weight substrates in vivo. J. Bacteriol. 173:2695-2703.
5. Baneyx, F., and G. Georgiou. 1992. Degradation of secreted proteins in Escherichia coli. Ann. N.Y. Acad. Sci. 665:301-308.
6. Benjelloun-Touimi, Z., P. J. Sansonetti, and C. Parsot. 1995. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17:123-135.
7. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coll. Infect. Immun. 57:1506-1511.
8. Benz, I., and M. A. Schmidt. 1992. AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27) is synthesized via a precursor molecule. Mol. Microbiol. 6:1539-1546.
9. Benz, L, and M. A. Schmidt. 1992. Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126:H27). Infect. Immun. 60:13-18.
10. Binet, R., S. Letoffe, J. M. Ghigo, P. Delepelaire, and C. Wandersman. 1997. Protein secretion by gram-negative bacterial ABC exporters - a review. Gene 192:7-11.
11. Charles, I., N. Failweather, D. Pickard, J. Beesley, R. Anderson, G. Dougan, and M. Roberts. 1994. Expression of the Bordetella pertussis P.69 pertactin adhesin in Escherichia coli: fate of the carboxy-terminal domain. Microbiology 140:3301-3308.
12. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
13. Cowan, S. W., T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, R. A. Pauptit, J. N. Jansonius, and J. P. Rosenbusch. 1992. Crystal structures explain functional properties of two E. coli porins. Nature 358:727-733.
14. de Cock, H., S. van Blokland, and J. Tommassen. 1996. In vitro insertion and assembly of outer membrane protein PhoE of Escherichia coli K-12 into the outer membrane. Role of Triton X-100. J. Biol. Chem. 271:12885-12890.
15. Elish, M. E., J. R. Pierce, and C. F. Earhart. 1988. Biochemical analysis of spontaneous fepA mutants of Escherichia coli. J. Gen. Microbiol. 134:1355-1364.
16. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
17. Galan, J. E. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
18. Garten, W., I. Hindennach, and U. Henning. 1975. The major proteins of the Escherichia coli outer cell envelope membrane. Characterization of proteins II* and III, comparison of all proteins. Eur. J. Biochem. 59:215-221.
19. Goldberg, M. B., O. Bârzu, C. Parsot, and P. J. Sansonetti. 1993. Unipolar localization and ATPase activity of IcsA, a Skigella flexneri protein involved in intracellular movement. J. Bacteriol. 175:2189-2196.
20. Haller, R., J. Pohlner, and T. F. Meyer. 1984. IgA protease of Neisseria gonorrhoeae: isolation and characterization of the gene and its extracellular product. EMBO J. 3:1595-1601.
21. Henderson, I. R., F. Navarrogarcia, and J. P. Nataro. 1998. The great escape - structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
22. Hendrixson, D. R., M. L. de la Morena, C. Stathopoulos, and J. W. St. Geme. 1997. Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol. Microbiol. 26:505-518.
23. Jose, J., F. Jahnig, and T. F. Meyer. 1995. Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol. Microbiol. 18:378-380.
24. Jose, J., J. Kramer, T. Klauser, J. Pohlner, and T. F. Meyer. 1996. Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Iga beta autotransporter pathway. Gene 178:107-110.
25. Klauser, T., J. Kramer, K. Otzelberger, J. Pohlner, and T. F. Meyer. 1993. Characterization of the Neisseria Iga beta-core. The essential unit for outer membrane targeting and extracellular protein secretion. J. Mol. Biol. 234: 579-593.
26. Klauser, T., J. Pohlner, and T. F. Meyer. 1990. Extracellular transport of cholera toxin B subunit using Neisseria IgA protease beta-domain: conformation-dependent outer membrane translocation. EMBO J. 9:1991-1999.
27. Klauser, T., J. Pohlner, and T. F. Meyer. 1992. Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Iga beta-mediated outer membrane transport. EMBO J. 11:2327-2335.
28. Klauser, T., J. Pohlner, and T. F. Meyer. 1993. The secretion pathway of IgA protease-type proteins in gram-negative bacteria. Bioessays 15:799-805.
29. Kubori, T., Y. Matsushima, D. Nakamura, J. Uralil, M. Laratejero, A. Sukhan, J. E. Galan, and S. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280:602-605.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Loveless, B. J., and M. H. Saier, Jr. 1997. A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14:113-123.
32. Ludwig, D. S., R. K. Holmes, and G. K. Schoolnik. 1985. Chemical and immunochemical studies on the receptor binding domain of cholera toxin B subunit. J. Biol. Chem. 260:12528-12534.
33. Maurer, J., J. Jose, and T. F. Meyer. 1997. Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. J. Bacteriol. 179:794-804.
34. Meyer, T. F., R. Halter, and J. Pohlner. 1987. Mechanism of extracellular secretion of an IgA protease by gram-negative host cells. Adv. Exp. Med. Biol. 216B:1271-1281.
35. Miyazaki, H., N. Yanagida, S. Horinouchi, and T. Beppu. 1989. Characterization of the precursor of Serratia marcescens serine protease and COOH-terminal processing of the precursor during its excretion through the outer membrane of Escherichia coli. J. Bacteriol. 171:6566-6572.
36. Murphy, C., W. Prinz, M. Pohlschroder, A. Derman, and J. Beckwith. 1995. Essential features of the pathway for protein translocation across the Escherichia coli cytoplasmic membrane. Cold Spring Harbor Symp. Quant. Biol. 60:277-283.
37. Ohnishi, Y., M. Nishiyama, S. Horinouchi, and T. Beppu. 1994. Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J. Biol. Chem. 269:32800-32806.
38. Pautsch, A., and G. E. Schulz. 1998. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5:1013-1017.
39. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458-462.
40. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
41. Pugsley, A. P., O. Francetic, O. M. Possot, N. Sauvonnet, and K. R, Hardie. 1997. Recent progress and future directions in studies of the main terminal branch of the general secretory pathway in gram-negative bacteria - a review. Gene 192:13-19.
42. Rosqvist, R., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1995. Functional conservation of the secretion and translocation machinery for virulence proteins of Yersiniae, Salmonellae and Shigellae. EMBO J. 14:4187-4195.
43. Salmond, G. P., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
44. Sambrook, J., E. F. Fritsch, and T. Manialis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
45. Schmitt, W., and R. Haas. 1994. Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol. Microbiol. 12:307-319.
46. Shikata, S., K. Shimada, Y. Ohnishi, S. Horinouchi, and T. Beppu. 1993. Characterization of secretory intermediates of Serratia marcescens serineprotease produced during its extracellular secretion from Escherichia-coli-cells. J. Biochem. 114:723-731.
47. Sugawara, E., M. Steiert, S. Rouhani, and H. Nikaldo. 1996. Secondary structure of the outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J. Bacteriol. 178:6067-6069.
48. Suhr, M., I. Benz, and M. A. Schmidt. 1996. Processing of the AIDA-1 precursor: removal of AIDAc and evidence for the outer membrane anchoring as a beta-barrel structure. Mol. Microbiol. 22:31-42.
49. Suzuki, T., M. C. Lett, and C. Sasakawa. 1995. Extracellular transport of VirG protein in Shigella. J. Biol. Chem. 270:30874-30880.
50. Van Gijsegem, F., S. Genin, and C. Boucher. 1993. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1:175-180.
51. Weiss, M. S., U. Abele, J. Weckesser, W. Welte, E. Schiltz, and G. E. Schulz. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627-1630.
52. Weiss, M. S., A. Kreusch, E. Schiltz, U. Nestel, W. Welte, J. Weckesser, and G.E. Schulz. 1991. The structure of porin from Rhodobacter capsulatus at 1.8 Å resolution. FEBS Lett. 280:379-382.
53. Welch, R. A. 1991. Pore-forming cytolysins of gram-negative bacteria. Mol. Microbiol. 5:521-528.
54. Yanagida, N., T. Uozumi, and T. Beppu. 1986. Specific excretion of Serratia marcescens protease through the outer membrane of Escherichia coli. J. Bacteriol. 166:937-944.