1887

Abstract

Typical enteropathogenic strains express an established virulence factor belonging to the type IV pili family, called the bundle-forming pilus (BFP). BFP are present on the cell surface as bundled filamentous appendages, and are assembled and retracted by proteins encoded by the operon. These proteins assemble to form a molecular machine. The BFP machine may be conceptually divided into three components: the cytoplasmic membrane (CM) subassembly, which is composed of CM proteins and cytoplasmic nucleotide-binding proteins; the outer membrane (OM) subassembly and the pilus itself. The authors have previously characterized the CM subassembly and the pilus. In this study, a more complete characterization of the OM subassembly was carried out using a combination of biochemical, biophysical and genetic approaches. It is reported that targeting of BfpG to the OM was influenced by the secretin BfpB. BfpG and BfpU interacted with the amino terminus of BfpB. BfpU had a complex cellular distribution pattern and, along with BfpB and BfpG, was part of the OM subassembly.

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2006-08-01
2024-03-28
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References

  1. Alberts B. 1998; The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92:291–294 [CrossRef]
    [Google Scholar]
  2. Alm R. A, Mattick J. S. 1997; Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa . Gene 192:89–98 [CrossRef]
    [Google Scholar]
  3. Anantha R. P, Stone K. D, Donnenberg M. S. 1998; The role of BfpF, a member of the PilT family of putative nucleotide-binding proteins, in type IV pilus biogenesis and in interactions between enteropathogenic Escherichia coli and host cells. Infect Immun 66:122–131
    [Google Scholar]
  4. Anantha R. P, Stone K. D, Donnenberg M. S. 2000; Effects of bfp mutations on biogenesis of functional enteropathogenic Escherichia coli type IV pili. J Bacteriol 182:2498–2506 [CrossRef]
    [Google Scholar]
  5. Baldini M. M, Kaper J. B, Levine M. M, Candy D. C, Moon H. W. 1983; Plasmid-mediated adhesion in enteropathogenic Escherichia coli . J Pediatr Gastroenterol Nutr 2:534–538 [CrossRef]
    [Google Scholar]
  6. Bieber D, Ramer S. W, Wu C. Y, Murray W. J, Tobe T, Fernandez R, Schoolnik G. K. 1998; Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli . Science 280:2114–2118 [CrossRef]
    [Google Scholar]
  7. Blank T. E, Donnenberg M. S. 2001; Novel topology of BfpE, a cytoplasmic membrane protein required for type IV fimbrial biogenesis in enteropathogenic Escherichia coli . J Bacteriol 183:4435–4450 [CrossRef]
    [Google Scholar]
  8. Bradley D. E. 1980; A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 26:146–154 [CrossRef]
    [Google Scholar]
  9. Chen I, Dubnau D. 2003; DNA transport during transformation. Front Biosci 8:s544–s556 [CrossRef]
    [Google Scholar]
  10. Crago A. M, Koronakis V. 1998; Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol Microbiol 30:47–56 [CrossRef]
    [Google Scholar]
  11. Craig L, Pique M. E, Tainer J. A. 2004; Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378 [CrossRef]
    [Google Scholar]
  12. Cravioto A, Gross R. J, Scotland S. M, Rowe B. 1979; An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr Microbiol 3:95–99 [CrossRef]
    [Google Scholar]
  13. Crowther L. J, Anantha R. P, Donnenberg M. S. 2004; The inner membrane subassembly of the enteropathogenic Escherichia coli bundle-forming pilus machine. Mol Microbiol 52:67–79 [CrossRef]
    [Google Scholar]
  14. Crowther L. J, Yamagata A, Craig L, Tainer J. A, Donnenberg M. S. 2005; The ATPase activity of BfpD is greatly enhanced by zinc and allosteric interactions with other Bfp proteins. J Biol Chem 280:24839–24848 [CrossRef]
    [Google Scholar]
  15. Datsenko K. A, Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [CrossRef]
    [Google Scholar]
  16. Donnenberg M. S, Kaper J. B. 1992; Minireview: enteropathogenic Escherichia coli . Infect Immun 60:3953–3961
    [Google Scholar]
  17. Donnenberg M. S, Nataro J. P, Kaper J. B, Girón J. A. 1992; A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6:3427–3437 [CrossRef]
    [Google Scholar]
  18. Donnenberg M. S, Zhang H.-Z, Stone K. D. 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 [CrossRef]
    [Google Scholar]
  19. Drake S. L, Sandstedt S. A, Koomey M. 1997; PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae , affects expression of PilQ as a high-molecular-mass multimer. Mol Microbiol 23:657–668 [CrossRef]
    [Google Scholar]
  20. Genin S, Boucher C. A. 1994; A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N- terminal domain. Mol Gen Genet 243:112–118 [CrossRef]
    [Google Scholar]
  21. Girón J. A, Ho A. S. Y, Schoolnik G. K. 1991; An inducible bundle-forming pilus of enteropathogenic Escherichia coli . Science 254:710–713 [CrossRef]
    [Google Scholar]
  22. Girón J. A, Qadri F, Azim T, Jarvis K. J, Kaper J. B, Albert M. J. 1995; Monoclonal antibodies specific for the bundle-forming pilus of enteropathogenic Escherichia coli . Infect Immun 63:4949–4952
    [Google Scholar]
  23. Guzman L. M, Belin D, Carson M. J, Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130
    [Google Scholar]
  24. Hardie K. R, Lory S, Pugsley A. P. 1996; Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J 15:978–988
    [Google Scholar]
  25. Henrichsen J. 1983; Twitching motility. Annu Rev Microbiol 37:81–93 [CrossRef]
    [Google Scholar]
  26. Herrington D. A, Hall R. H, Losonsky G, Mekalanos J. J, Taylor R. K, Levine M. M. 1988; Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J Exp Med 168:1487–1492 [CrossRef]
    [Google Scholar]
  27. Hobbs M, 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 [CrossRef]
    [Google Scholar]
  28. Hottenrott S, Schumann T, Pluckthun A, Fischer G, Rahfeld J. U. 1997; The Escherichia coli SlyD is a metal ion-regulated peptidyl-prolyl cis/trans -isomerase. J Biol Chem 272:15697–15701 [CrossRef]
    [Google Scholar]
  29. Hwang J, Bieber D, Ramer S. W, Wu C. Y, Schoolnik G. K. 2003; Structural and topographical studies of the type IV bundle-forming pilus assembly complex of enteropathogenic Escherichia coli . J Bacteriol 185:6695–6701 [CrossRef]
    [Google Scholar]
  30. Koebnik R, Locher K. P, Van Gelder P. 2000; Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253 [CrossRef]
    [Google Scholar]
  31. Lee K. K, Sheth H. B, Wong W. Y, Sherburne R, Paranchych W, Hodges R. S, Lingwood C. A, Krivan H, Irvin R. T. 1994; The binding of Pseudomonas aeruginosa pili to glycosphingolipids is a tip-associated event involving the C -terminal region of the structural pilin subunit. Mol Microbiol 11:705–713 [CrossRef]
    [Google Scholar]
  32. Levine M. M, Bergquist E. J, Nalin D. R, Waterman D. H, Hornick R. B, Young C. R, Sotman S, Rowe B. 1978; Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1:1119–1122
    [Google Scholar]
  33. McNamara B. P, Koutsouris A, O'Connell C. B, Nougayrède J. P, Donnenberg M. S, Hecht G. 2001; Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 107:621–629 [CrossRef]
    [Google Scholar]
  34. Merz A. J, So M, Sheetz M. P. 2000; Pilus retraction powers bacterial twitching motility. Nature 407:98–102 [CrossRef]
    [Google Scholar]
  35. O'Connell C. B, Creasey E. A, Knutton S. 7 other authors 2004; SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 52:1613–1625 [CrossRef]
    [Google Scholar]
  36. Osborn M. J, Gander J. E, Parisi E, Carson J. 1972; Mechanism of assembly of the outer membrane of Salmonella typhimurium . Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247:3962–3972
    [Google Scholar]
  37. O'Toole G. A, Kolter R. 1998; Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304 [CrossRef]
    [Google Scholar]
  38. Peabody C. R, Chung Y. J, Yen M. R, Vidal-Ingigliardi D, Pugsley A. P, Saier M. H. Jr 2003; Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051–3072 [CrossRef]
    [Google Scholar]
  39. Phizicky E, Bastiaens P. I, Zhu H, Snyder M, Fields S. 2003; Protein analysis on a proteomic scale. Nature 422:208–215 [CrossRef]
    [Google Scholar]
  40. Ramboarina S, Fernandes P. J, Daniell S, Islam S, Simpson P, Frankel G, Booy F, Donnenberg M. S, Matthews S. 2005; Structure of the bundle-forming pilus from enteropathogenic Escherichia coli . J Biol Chem 280:40252–40260 [CrossRef]
    [Google Scholar]
  41. Ramer S. W, Bieber D, Schoolnik G. K. 1996; BfpB, an outer membrane lipoprotein required for the biogenesis of bundle-forming pili in enteropathogenic Escherichia coli . J Bacteriol 178:6555–6563
    [Google Scholar]
  42. Ramer S. W, Schoolnik G. K, Wu C. Y, Hwang J, Schmidt S. A, Bieber D. 2002; The type IV pilus assembly complex: biogenic interactions among the bundle-forming pilus proteins of enteropathogenic Escherichia coli . J Bacteriol 184:3457–3465 [CrossRef]
    [Google Scholar]
  43. Roof W. D, Fang H. Q, Young K. D, Sun J, Young R. 1997; Mutational analysis of slyD , an Escherichia coli gene encoding a protein of the FKBP immunophilin family. Mol Microbiol 25:1031–1046 [CrossRef]
    [Google Scholar]
  44. Rudel T, Scheuerpflug I, Meyer T. F. 1995; Neisseria PilC protein identified as type-4 pilus tip- located adhesin. Nature 373:357–359 [CrossRef]
    [Google Scholar]
  45. Russel M. 1998; Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J Mol Biol 279:485–499 [CrossRef]
    [Google Scholar]
  46. Sandkvist M. 2001; Biology of type II secretion. Mol Microbiol 40:271–283 [CrossRef]
    [Google Scholar]
  47. Scaletsky I. C. A, Silva M. L. M, Trabulsi L. R. 1984; Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 45:534–536
    [Google Scholar]
  48. Schmidt S. A, Bieber D, Ramer S. W, Hwang J, Wu C. Y, Schoolnik G. 2001; Structure-function analysis of BfpB, a secretin-like protein encoded by the bundle-forming-pilus operon of enteropathogenic Escherichia coli . J Bacteriol 183:4848–4859 [CrossRef]
    [Google Scholar]
  49. Schreiber W, Stone K. D, Strong M. A, Hoppert M, Donnenberg M. S, DeTolla L. J., Jr. 2002; BfpU, a soluble protein essential for type IV pilus biogenesis in enteropathogenic Escherichia coli . Microbiology 148:2507–2518
    [Google Scholar]
  50. Seifert H. S, Ajioka R. S, Marchal C, Sparling P. F, So M. 1988; DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae . Nature 336:392–395 [CrossRef]
    [Google Scholar]
  51. Shevchik V. E, Robert-Baudouy J, 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 [CrossRef]
    [Google Scholar]
  52. Sohel I, Puente J. L, Murray W. J, Vuopio-Varkila J, Schoolnik G. K. 1993; Cloning and characterization of the bundle-forming pilin gene of enteropathogenic Escherichia coli and its distribution in Salmonella serotypes. Mol Microbiol 7:563–575 [CrossRef]
    [Google Scholar]
  53. Stone B. J, Abu Kwaik Y. 1998; Expression of multiple pili by Legionella pneumophila : identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect Immun 66:1768–1775
    [Google Scholar]
  54. Stone K. D, Zhang H.-Z, Carlson L. K, Donnenberg M. S. 1996; A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for biogenesis of a type IV pilus. Mol Microbiol 20:325–337 [CrossRef]
    [Google Scholar]
  55. Strom M. S, Lory S. 1993; Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 47:565–596 [CrossRef]
    [Google Scholar]
  56. Strom M. S, Nunn D. N, 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 U S A 90:2404–2408 [CrossRef]
    [Google Scholar]
  57. Tacket C. O, Taylor R. K, Losonsky G, Lim Y, Nataro J. P, Kaper J. B, Levine M. M. 1998; Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect Immun 66:692–695
    [Google Scholar]
  58. Taniguchi T, Fujino Y, Yamamoto K, Miwatani T, Honda T. 1995; Sequencing of the gene encoding the major pilin of pilus colonization factor antigen III (CFA/III) of human enterotoxigenic Escherichia coli and evidence that CFA/III is related to type IV pili. Infect Immun 63:724–728
    [Google Scholar]
  59. Vuopio-Varkila J, Schoolnik G. K. 1991; Localized adherence by enteropathogenic Escherichia coli is an inducible phenotype associated with the expression of new outer membrane proteins. J Exp Med 174:1167–1177 [CrossRef]
    [Google Scholar]
  60. Wall D, Kaiser D. 1999; Type IV pili and cell motility. Mol Microbiol 32:1–10 [CrossRef]
    [Google Scholar]
  61. Wolfgang M, Lauer P, Park H. S, Brossay L, Koomey M, Hébert J. 1998; PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae . Mol Microbiol 29:321–330 [CrossRef]
    [Google Scholar]
  62. Wolfgang M, Hayes S. F, Dorward D, Koomey M, van Putten J. P. 2000; Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 19:6408–6418 [CrossRef]
    [Google Scholar]
  63. Yen M. R, Peabody C. R, Partovi S. M, Zhai Y, Tseng Y. H, Saier M. H. 2002; Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562:6–31 [CrossRef]
    [Google Scholar]
  64. Yoshida T, Kim S. R, Komano T. 1999; Twelve pil genes are required for biogenesis of the R64 thin pilus. J Bacteriol 181:2038–2043
    [Google Scholar]
  65. Zhang H.-Z, Donnenberg M. S. 1996; DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli . Mol Microbiol 21:787–797 [CrossRef]
    [Google Scholar]
  66. Zhang H.-Z, Lory S, Donnenberg M. S. 1994; A plasmid-encoded prepilin peptidase gene from enteropathogenic Escherichia coli . J Bacteriol 176:6885–6891
    [Google Scholar]
  67. Zhang X. L, Tsui I. S, Yip C. M, Fung A. W, Wong D. K, Dai X, Yang Y, Hackett J, Morris C. 2000; Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun 68:3067–3073 [CrossRef]
    [Google Scholar]
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