Type II protein secretion in Pseudomonas aeruginosa: The pseudopilus is a multifibrillar and adhesive structure

Journal of Bacteriology

Volumn 185, Issue 9, 2003, Pages 2749-2758

  Durand, Éric ^a   Bernadac, Alain ^a   Ball, Geneviève ^a   Lazdunski, Andrée ^a   Sturgis, James N ^a   Filloux, Alain ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ELASTASE; PROTEIN SUBUNIT; PSEUDOMONAS EXOTOXIN; UNCLASSIFIED DRUG; XCP SECRETON;

ARTICLE; BACTERIUM ADHERENCE; BACTERIUM PILUS; CONTROLLED STUDY; MACROMOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; PSEUDOPILUS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON; PSEUDOMONAS AERUGINOSA; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0037406829     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.9.2749-2758.2003     Document Type: Article

References (42)

1. Ball, G., E. Durand, A. Lazdunski, and A. Filloux. 2002. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43:475-485.
2. Bally, M., A. Filloux, M. Akrim, G. Ball, A. Lazdunski, and J. Tommassen. 1992. Protein secretion in Pseudomonas aeruginosa: characterization of seven xcp genes and processing of secretory apparatus components by prepilin peptidase. Mol. Microbiol. 6:1121-1131.
3. Bitter, W., M. Koster, M. Latijnhouwers, H. de Cock, and J. Tommassen. 1998. Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol. Microbiol. 27:209-219.
4. Bitter, W., and J. Tommassen. 1999. Ushers and other doorkeepers. Trends Microbiol. 7:4-6.
5. Bleves, S., M. Gerard-Vincent, A. Lazdunski, and A. Filloux. 1999. Structure-function analysis of XcpP, a component involved in general secretory pathway-dependent protein secretion in Pseudomonas aeruginosa. J. Bacteriol. 181:4012-4019.
6. Bleves, S., R. Voulhoux, G. Michel, A. Lazdunski, J. Tommassen, and A. Filloux. 1998. The secretion apparatus of Pseudomonas aeruginosa: identification of a fifth pseudopilin, XcpX (GspK family). Mol. Microbiol. 27:31-40.
7. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
8. Crowther, R. A., R. Henderson, and J. M. Smith. 1996. MRC image processing programs. J. Struct. Biol. 116:9-16.
9. Deziel, E., Y. Comeau, and R. Villemur. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183:1195-1204.
10. Donnenberg, M. S., H. Z. Zhang, and K. D. Stone. 1997. Biogenesis of the bundle-forming pilus of enteropathogenic Escherichia coli: reconstitution of fimbriae in recombinant E. coli and role of DsbA in pilin stability - a review. Gene 192:33-38.
11. Filloux, A., M. Bally, G. Ball, M. Akrim, J. Tommassen, and A. Lazdunski. 1990. Protein secretion in gram-negative bacteria: transport across the outer membrane involves common mechanisms in different bacteria. EMBO J. 9:4323-4329.
12. Filloux, A., G. Michel, and M. Bally. 1998. GSP-dependent protein secretion in gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol. Rev. 22:177-198.
13. Finelli, A., C. V. Gallant, K. Jarvi, and L. L. Burrows. 2003. Use of in-biofilm expression technology to identify genes involved in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185:2700-2710.
14. Forest, K. T., and J. A. Tainer. 1997. Type-4 pilus-structure: outside to inside and top to bottom - a minireview. Gene 192:165-169.
15. Gérard-Vincent, M., V. Robert, G. Ball, S. Bleves, G. P. F. Michel, A. Lazdunski, and A. Filloux. 2002. Identification of XcpP domains that confer functionality and specificity to the Pseudomonas aeruginosa type II secretion apparatus. Mol. Microbiol. 44:1651-1665.
16. Giron, J. A., O. G. Gomez-Duarte, K. G. Jarvis, and J. B. Kaper. 1997. Longus pilus of enterotoxigenic Escherichia coli and its relatedness to other type-4 pili - a minireview. Gene 192:39-43.
17. Govan, J. R., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
18. Hobbs, M., and J. S. Mattick. 1993. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol. Microbiol. 10:233-243.
19. Hoyne, P. A., R. Haas, T. F. Meyer, J. K. Davies, and T. C. Elleman. 1992. Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa. J. Bacteriol. 174:7321-7327.
20. Hu, N. T., W. M. Leu, M. S. Lee, A. Chen, S. C. Cheng, Y. L. Song, and L. Y. Chen. 2002. XpsG, the major pseudopilin in Xanthomonas campestris pv. campestris, forms pilus-like structure between cytoplasmic and outer membranes. Biochem. J. 365:205-211.
21. Kachlany, S. C., P. J. Planet, R. DeSalle, D. H. Fine, and D. H. Figurski. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol. 9:429-437.
22. Keizer, D. W., C. M. Slupsky, M. Kalisiak, A. P. Campbell, M. P. Crump, P. A. Sastry, B. Hazes, R. T. Irvin, and B. D. Sykes. 2001. Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J. Biol. Chem. 276:24186-24193.
23. Nunn, D., S. Bergman, and S. Lory. 1990. Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J. Bacteriol. 172:2911-2919.
24. Nunn, D. N., and S. Lory. 1991. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl. Acad. Sci. USA 88:3281-3285.
25. Nunn, D. N., and S. Lory. 1993. Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W. J. Bacteriol. 175:4375-4382.
26. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
27. Parge, H. E., K. T. Forest, M. J. Hickey, D. A. Christensen, E. D. Getzoff, and J. A. Tainer. 1995. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378:32-38.
28. Planet, P. J., S. C. Kachlany, R. DeSalle, and D. H. Figurski. 2001. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA 98:2503-2508.
29. Possot, O. M., G. Vignon, N. Bomchil, F. Ebel, and A. P. Pugsley. 2000. Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J. Bacteriol. 182:2142-2152.
30. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
31. Pugsley, A. P. 1996. Multimers of the precursor of a type IV pilin-like component of the general secretory pathway are unrelated to pili. Mol. Microbiol. 20:1235-1245.
32. Rahme, L. G., F. M. Ausubel, H. Cao, E. Drenkard, B. C. Goumnerov, G. W. Lau, S. Mahajan-Miklos, J. Plotnikova, M. W. Tan, J. Tsongalis, C. L. Walendziewicz, and R. G. Tompkins. 2000. Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. USA 97:8815-8821.
33. Sauvonnet, N., P. Gounon, and A. P. Pugsley. 2000. PpdD type IV pilin of Escherichia coli K-12 can be assembled into pili in Pseudomonas aeruginosa. J. Bacteriol. 182:848-854.
34. Sauvonnet, N., G. Vignon, A. P. Pugsley, and P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
35. Simpson, D. A., R. Ramphal, and S. Lory. 1992. Genetic analysis of Pseudomonas aeruginosa adherence: distinct genetic loci control attachment to epithelial cells and mucins. Infect. Immun. 60:3771-3779.
36. Smith, A. W., and B. H. Iglewski. 1989. Transformation of Pseudomonas aeruginosa by electroporation. Nucleic Acids Res. 17:10509.
37. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, and I. T. Paulsen. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964.
38. Tommassen, J., A. Filloux, M. Bally, M. Murgier, and A. Lazdunski. 1992. Protein secretion in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 9:73-90.
39. Vallet, I., J. W. Olson, S. Lory, A. Lazdunski, and A. Filloux. 2001. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 98:6911-6916.
40. Voulhoux, R., G. Ball, B. Ize, M. L. Vasil, A. Lazdunski, L. F. Wu, and A. Filloux. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 20:6735-6741.
41. Wall, D., and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10.
42. Wolfgang, M., J. P. van Putten, S. F. Hayes, D. Dorward, and M. Koomey. 2000. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 19:6408-6418.