Pilus formation and protein secretion by the same machinery in Escherichia coli

EMBO Journal

Volumn 19, Issue 10, 2000, Pages 2221-2228

  Sauvonnet, Nathalie ^c   Vignon, Guillaume ^a   Pugsley, Anthony P ^a   Gounon, Pierre ^b  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

General secretory pathway; Pili; Protein secretion; Secretin; Secreton

Indexed keywords

PULLULANASE;

ARTICLE; BACTERIUM PILUS; BIOGENESIS; ESCHERICHIA COLI; KLEBSIELLA OXYTOCA; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; KLEBSIELLA OXYTOCA; NEGIBACTERIA;

EID: 0034657719     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.10.2221     Document Type: Article

References (49)

1. Alm, R.A. and Mattick, J.S. (1995) Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol. Microbiol., 16, 485-496.
2. Alm, R.A. and Mattick, J.S. (1997) Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa. Gene, 192, 89-98.
3. Beard, M.K., Mattick, J.S., Moor, M.R., Marrs, C.F. and Egerton, J.R. (1990) Morphogenic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa. J. Bacteriol., 172, 2601-2607.
4. Bieber, D., Ramer, S., Wu, C., Murray, W., Tobe, T., Fernandez, R. and Schoolnik, G. (1998) Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science, 280, 2114-2118.
5. Bitter, W., Koster, M., Latijnhouwers, M., de Cock, H. and Tommassen, J. (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.
6. Bleves, S., Lazdunski, A., Tommassen, J. and Filloux, A. (1998) The secretion apparatus of Pseudomonas aeruginosa: identification of a fifth pseudopilin, XcpX. Mol. Microbiol., 27, 31-40.
7. d'Enfert, C., Chapon, C. and Pugsley, A.P. (1987a) Export and secretion of the lipoprotein pullulanase by Klebsiella pneumoniae. Mol. Microbiol., 1, 107-116.
8. d'Enfert, C., Ryter, A. and Pugsley, A.P. (1987b) Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J., 6, 3531-3538.
9. Drake, S.L. and Koomey, M. (1995) The product of the pilQ gene is essential for biogenesis of type IV pili in Neisseria gonorrhoeae. Mol. Microbiol., 18, 975-986.
10. Drake, S.L., Sandstedt, S.A. and Koomey, M. (1997) PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhneae, affects expression of PilQ as a high-molecular-mass multimer. Mol. Microbiol., 23, 657-668.
11. Elleman, T.C., Hoyne, P.A., Stewart, D.J., McKern, N.M. and Peterson, J.E. (1986) Expression of pili from Bacteroides nodosus in Pseudomonas aeruginosa. J. Bacteriol., 168, 574-580.
12. Folkhard, W., Marvin, D.A., Watts, T.H. and Paranchych, W. (1981) Structure of polar pili from Pseudomonas aeruginosa strains K and O. J. Mol. Biol. 149, 79-93.
13. Guilvout, I., Hardie, K.R., Sauvonnet, N. and Pugsley, A.P. (1999) Genetic dissection of the outer membrane secretin PulD: are there distinct domains for multimerization and secretion specificity? J. Bacteriol., 181, 7212-7220.
14. Hardie, K.R., Lory, S. and Pugsley, A.P. (1996a) Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J., 15, 978-988.
15. Hardie, K.R., Seydel, A., Guilvout, I. and Pugsley, A.P. (1996b) The secretin-specific, chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions. Mol. Microbiol., 22, 967-976.
16. Hobbs, M. and Mattick, J.S. (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.
17. Kagami, Y., Ratliff, M., Surber, M., Martinez, A. and Nunn, D. (1998) Type II protein secretion by Pseudomonas aeruginosa: genetic suppression of a conditional mutation in the pilin-like component XcpT by the cytoplasmic component XcpR. Mol. Microbiol., 27, 221-233.
18. Kirov, S.M., O'Donovan, L.M. and Sanderson, K. (1999) Functional characterization of type IV pili expressed on diarrhoea-associated isolates of Aeromonas species. Infect. Immun., 67, 5447-5454.
19. Lindeberg, M., Salmond, G.P.C. and Collmer, A. (1996) Complementation of deletion mutations in a cloned functional cluster of Erwinia chrysanthemi out genes with Erwinia carotovora out homologs reveals OutC and OutD as candidate gatekeepers of species-specific secretion of proteins via the type II pathway. Mol. Microbiol., 20, 175-190.
20. Lopilato, J., Bortner, S. and Beckwith, J. (1986) Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives. Mol. Gen. Genet., 205, 285-290.
21. Lu, H.-M., Motley, S.T. and Lory, S. (1997) Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion. Mol. Microbiol., 25, 247-259.
22. Martin, P.R., Hobbs, M., Free, P.D., Jeske, Y. and Mattick, J.S. (1993) Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol., 9, 857-868.
23. Mattick, J.S., Bills, M.M., Anderson, B.J., Dalrymple, B., Mott, M.R. and Egerton, J.R. (1987) Morphogenic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J. Bacteriol., 169, 33-41.
24. Michaelis, S., Chapon, C., d'Enfert, C., Pugsley, A.P. and Schwartz, M. (1985) Characterization and expression of the structural gene for pullulanase, a maltose-inducible secreted protein of Klebsiella pneumonia. J. Bacteriol., 164, 633-638.
25. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Nouwen, N., Ranson, N., Saibil, H., Wolpensinger, B., Engel, A., Ghazi, A. and Pugsley, A.P. (1999) Secretin PulD: association with pilot protein PulS, structure and ion-conducting channel formation. Proc. Natl Acad. Sci. USA, 96, 8173-8177.
27. Nunn, D. (1999) Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol., 9, 402-408.
28. Nunn, D. and Lory, S. (1991) Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl Acad. Sci. USA, 88, 3281-3285.
29. Nunn, D. and Lory, S. (1992) Components of the protein excretion apparatus of Pseudomonas aeruginosa are processed by the type IV prepilin peptidase. Proc. Natl Acad. Sci. USA, 89, 47-51.
30. Nunn, D., Bergman, S. and Lory, S. (1990) Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J. Bacteriol., 172, 2911-2919.
31. Parge, H.E. et al. (1990) Biochemical purification and crystallographic characterization of the fiber-forming protein pilin from Neisseria gonorrhoeae. J. Bacteriol., 265, 2278-2285.
32. Parge, H.E., Forest, K.T., Hickey, M.J., Christensen, D.A., Getzoff, E.D. and Tainer, J.A. (1995) Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature, 378, 32-38.
33. Possot, O. and Pugsley, A.P. (1994) Molecular characterization of PulE, a protein required for pullulanase secretion. Mol. Microbiol., 12, 287-299.
34. Possot, O., d'Enfert, C., Reyss, I. and Pugsley, A.P. (1992) Pullulanase secretion in Escherichia coli K12 requires a cytoplasmic protein and a putative polytopic cytoplasmic membrane protein. Mol. Microbiol., 6, 95-105.
35. Possot, O.M., Gérard, M. and Pugsley, A.P. (1999) Membrane association and multimerization of secreton component PulC. J. Bacteriol., 181, 4004-4011.
36. Possot, O., Vignon, G., Bomchil, N., Ebel, F. and Pugsley, A.P. (2000) Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J. Bacteriol., 182, 2142-2152.
37. Pugsley, A.P. (1993a) The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev., 57, 50-108.
38. Pugsley, A.P. (1993b) Processing and methylation of PulG, a pilin-like component of the general secretory pathway of Klebsiella oxytoca. Mol. Microbiol., 9, 295-308.
39. 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.
40. Pugsley, A.P. and Possot, O. (1993) The general secretory pathway of Klebsiella oxytoca: no evidence for relocalization or assembly of pilin-like PulG protein into a multiprotein complex. Mol. Microbiol., 10, 665-674.
41. Pugsley, A.P., Kornacker, M.G. and Ryter, A. (1990) Analysis of the subcellular location of pullulanase produced by Escherichia coli carrying the pulA gene from Klebsiella pneumoniae strain UNF5023. Mol. Microbiol., 4, 59-72.
42. Reyss, I. and Pugsley, A.P. (1990) Five additional genes in the pulC-O operon of the Gram-negative bacterium Klebsiella oxytoca UNF5023 that are required for pullulanase secretion. Mol. Gen. Genet., 222, 176-184.
43. Roine,E., Wei, W., Yuan, J., Nurmiaho-Lassila, E.L., Kalkkinen, N., Romantschuk, M. and He, S.Y. (1997) Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl Acad. Sci. USA, 94, 3459-3464.
44. Russel, M.M. and Darzins, A. (1994) The pilE gene of Pseudomonas aeruginosa, required for pilus biogenesis, shares amino acid sequence identity with the N-termini of type 4 prepilin proteins. Mol. Microbiol., 13, 973-985.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Sauvonnet, N., Gounon, P. and Pugsley, A.P. (2000) PpdD type IV pilin of Escherichia coli K-12 can be assembled into pili in Pseudomonas aeruginosa. J. Bacteriol., 182, 848-854.
47. Shevchik, V.E., Robert-Badouy, J. and Condemine, G. (1997) Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO J., 16, 3007-3016.
48. Strom, M.S., Nunn, D.N. and Lory, S. (1993) A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl Acad. Sci. USA, 90, 2404-2408.
49. Young, G.M., Schmiel, D.H. and Miller, V.L. (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl Acad. Sci. USA, 96, 6456-6461.