Type IV pilus structure and bacterial pathogenicity

Nature Reviews Microbiology

Volumn 2, Issue 5, 2004, Pages 363-378

  Craig, Lisa ^a   Pique, Michael E ^a   Tainer, John A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; PILIN; PROTEIN SUBUNIT; FIMBRIA PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; APOPTOSIS; AZOARCUS; BACTERIAL CELL; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM PILUS; CELL STRUCTURE; CELL SURFACE; CITROBACTER; COLONY FORMATION; COMPLEMENT INHIBITION; DICHELOBACTER NODOSUS; DIFFRACTION; DRUG TARGETING; EIKENELLA CORRODENS; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; IMMUNE RESPONSE; MOLECULAR MECHANICS; MORAXELLA; MYCOBACTERIUM BOVIS; MYXOCOCCUS XANTHUS; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA TYPHI; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; X RAY CRYSTALLOGRAPHY; BACTERIUM ADHERENCE; CHEMICAL STRUCTURE; CHEMISTRY; FIMBRIA; GENETIC TRANSDUCTION; IMMUNOLOGY; PATHOGENICITY; PHYSIOLOGY;

AZOARCUS; BACTERIA (MICROORGANISMS); CITROBACTER; DICHELOBACTER NODOSUS; EIKENELLA CORRODENS; ESCHERICHIA COLI; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYXOCOCCUS XANTHUS; NEGIBACTERIA; NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SALMONELLA; SALMONELLA TYPHI; VIBRIO; VIBRIO CHOLERAE;

BACTERIAL ADHESION; CRYSTALLOGRAPHY, X-RAY; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GRAM-NEGATIVE BACTERIA; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; NEISSERIA GONORRHOEAE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; TRANSDUCTION, GENETIC; VIBRIO CHOLERAE;

EID: 2442589577     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro885     Document Type: Review

References (150)

1. Levine, M. M. et al. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152, 550-559 (1985).
2. Herrington, D. A. et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168, 1487-1492 (1988).
3. Tacket, C. O. et al. 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 (1998).
4. Bieber, D. et al. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280, 2114-2118 (1998).
5. Maier, B., Potter, L., So, M., Seifert, H. S. & Sheetz, M. P. Single pilus motor forces exceed 100 pN. Proc. Natl Acad. Sci. USA 99, 16012-16017 (2002).
6. Merz, A. J., So, M. & Sheetz, M. P. Pilus retraction powers bacterial twitching motility. Nature 407, 98-102 (2000).
7. Bragg, S. L. The Development of X-ray Analysis (eds Phillips, D. C. & Lipson, H.) (G. Bell, London, 1975).
8. Schutt, C. E., Myslik, J. C., Rozycki, M. D., Goonesekere, N. C. & Lindberg, U. The structure of crystalline profilin-β-actin. Nature 365, 810-816 (1993).
9. Kabsch, W., Mannherz, H. G. & Suck, D. Three-dimensional structure of the complex of actin and DNase I at 4.5 Å resolution. EMBO J. 4, 2113-2118 (1985).
10. McLaughlin, P. J., Gooch, J. T., Mannherz, H. G. & Weeds, A. G. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing. Nature 364, 685-692 (1993).
11. Robinson, R. C. et al. Domain movement in gelsolin: a calcium-activated switch. Science 286, 1939-1942 (1999).
12. Otterbein, L. R., Graceffa, P. & Dominguez, R. The crystal structure of uncomplexed actin in the ADP state. Science 293, 708-711 (2001).
13. Rayment, I. et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58 (1993).
14. Samatey, F. A. et al. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410, 331-337 (2001).
15. Sauer, F. G. et al. Structural basis of chaperone function and pilus biogenesis. Science 285, 1058-1061 (1999).
16. Craig, L. et al. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol. Cell. 11, 1139-1150 (2003).
17. Parge, H. E. et al. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378, 32-38 (1995).
18. Hazes, B., Sastry, P. A., Hayakawa, K., Read, R. J. & Irvin, R. T. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J. Mol. Biol. 299, 1005-1017 (2000).
19. Keizer, D. W. et al. Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J. Biol. Chem. 276, 24186-24193 (2001).
20. Yonekura, K., Maki-Yonekura, S. & Namba, K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424, 643-650 (2003).
21. Li, H., DeRosier, D., Nicholson, W., Nogales, E. & Downing, K. Microtubule structure at 8 Å resolution. Structure 10, 1317 (2002).
22. Zhu, Y., Carragher, B., Kriegman, D. J., Milligan, R. A. & Potter, C. S. Automated identification of filaments in cryo-electron microscopy images. J. Struct. Biol. 135, 302-312 (2001).
23. Pauling, L. & Corey, R. B. Two hydrogen-bonded spiral configurations of the polypeptide chain. J. Am. Chem. Soc. 72 534 (1950).
24. Franklin, R. & Gosling, R. G. Molecular configuration in sodium thymonucleate. Nature 171, 740-741 (1953).
25. Watson, J. D. & Crick, F. H. C. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737-738 (1953).
26. Kishchenko, G., Batliwala, H. & Makowski, L. Structure of a foreign peptide displayed on the surface of bacteriophage M13. J. Mol. Biol. 241, 208-213 (1994).
27. Bryan, R. K., Bansal, M., Folkhard, W., Nave, C. & Marvin, D. A. Maximum-entropy calculation of the electron density of 4 Å resolution A Pf1 filamentous bacteriophage. Proc. Natl Acad. Sci. USA 80, 4728-4731 (1983).
28. Peterson, C., Winter, W. T., Dalack, G. W. & Day, L. A. Structure of the filamentous bacteriophage, Pf3, by X-ray fiber diffraction. J. Mol. Biol. 162, 877-881 (1982).
29. Marvin, D. A., Nadassy, K., Welsh, L. C. & Forest, K. Type-4 bacterial pili: molecular models and their simulated diffraction patterns. Fibre Diffract. Rev. 11, 87-94 (2003).
30. Marvin, D. A. & Folkhard, W. Structure of F-pili: reassessment of the symmetry. J. Mol. Biol. 191, 299-300 (1986).
31. Serpell, L. C., Berriman, J., Jakes, R., Goedert, M. & Crowther, R. A. Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation. Proc. Natl Acad. Sci. USA 97, 4897-4902 (2000).
32. Perutz, M. F., Finch, J. T., Berriman, J. & Lesk, A. Amyloid fibers are water-filled nanotubes. Proc. Natl Acad. Sci. USA 99 5591-5595 (2002).
33. Morozova-Roche, L. A. et al. Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants. J. Struct. Biol. 130, 339-351 (2000).
34. Inouye, H. et al. Analysis of X-ray diffraction patterns from amyloid of biopsied vitreous humor and kidney of transthyretin (TTR) Met30 familial amyloidotic polyneuropathy (FAP) patients: axially arrayed TTR monomers constitute the protofilament. Amyloid 5, 163-174 (1998).
35. Folkhard, W., Marvin, D. A., Watts, T. H. & Paranchych, W. Structure of polar pili from Pseudomonas aeruginosa strains K and O. J. Mol. Biol. 149, 79-93 (1981).
36. Swanson, J. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J. Exp. Med. 137, 571-589 (1973).
37. Potts, W. J. & Saunders, J. R. Nucleotide sequence of the structural gene for class I pilin from Neisseria meningitidis: homologies with be pilF locus of Neisseria gonorrhoeae. Mol. Microbiol. 2, 647-653 (1988).
38. Meyer, T. F., Billyard, E., Haas, R., Storzbach, S. & So, M. Pilus genes of Neisseria gonorrheae: chromosomal organization and DNA sequence. Proc. Natl Acad. Sci. USA 81, 6110-6114 (1984).
39. Bradley, D. E. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can. J. Microbiol. 26, 146-154 (1980).
40. Woods, D. E., Straus, D. C., Johanson, W. G. Jr, Berry, V. K. & Bass, J. A. Role of pili in adherence of Pseudomonas aeruginosa to mammalian buccal epithelial cells. Infect. Immun. 29, 1146-1151 (1980).
41. Johnson, K., Parker, M. L. & Lory, S. Nucleotide sequence and transcriptional initiation site of two Pseudomonas aeruginosa pilin genes. J. Biol. Chem. 261, 15703-15708 (1986).
42. McKern, N. M., Stewart, D. J. & Strike, P. M. Amino acid sequences of pilins from serologically distinct strains of Bacteroides nodosus. J. Protein Chem. 7, 157-164 (1988).
43. Marrs, C. F. et al. Cloning and sequencing of a Moraxella bovis pilin gene. J. Bacteriol. 163, 132-139 (1985).
44. Tonjum, T., Marrs, C. F., Rozsa, F. & Bovre, K. The type 4 pilin of Moraxella nonliquefaciens exhibits unique similarities with the pilins of Neisseria gonorhoeae and Dichelobacter (Bacteroides) nodosus. J. Gen. Microbiol. 137, 2483-2490 (1991).
45. Tonjum, T., Weir, S., Bovre, K., Progulske-Fox, A. & Marrs, C. F. Sequence divergence in two tandemly located pilin genes of Eikenella corrodens. Infect. Immun. 61, 1909-1916 (1993).
46. Dorr, J., Hurek, T. & Reinhold-Hurek, B. Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol. 30, 7-17 (1998).
47. Rendulic, S. et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303, 689-692 (2004).
48. Faast, R., Ogierman, M. A., Stroeher U. H. & Manning, P. A. Nucleotide sequence of the structural gene, tcpA, for a major pilin subunit of Vibrio cholerae. Gene 85, 227-231 (1989).
49. Shaw, C. E. & Taylor, R. K. Vibrio cholerae O395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins. Infect. Immun. 58 3042-3049 (1990).
50. Zhang, X. L. et al. Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. Infect. Immun. 68, 3067-3073 (2000).
51. Donnenberg, M. S., Giron, J. A., Nataro, J. P. & Kaper, J. B. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6, 3427-3437 (1992).
52. Giron, J. A., Ho, A. S. & Schoolnik, G. K. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254, 710-713 (1991).
53. Taniguchi, T., Fujino, Y., Yamamoto, K., Miwatani, T. & Honda, T. Sequencing of the gene encoding to 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 (1995).
54. Giron, J. A., Levine, M. M. & Kaper, J. B. Longus: a long pilus ultrastructure produced by human enterotoxigenic Escherichia coli. Mol. Microbiol. 12, 71-82 (1994).
55. Pasloske, B. L., Scraba, D. G. & Paranchych, W. Assembly of mutant pilins in Pseudomonas aeruginosa: formation of pili composed of heterologous subunits. J. Bacteriol. 171, 2142-2147 (1989).
56. Strom, M. S. & Lory, S. Amino acid substitutions in pilin of Pseudomonas aeruginosa. Effect on leader peptide cleavage, amino-terminal methylation, and pilus assembly. J. Biol. Chem. 266, 1656-1664 (1991).
57. Macdonald, D. L., Pasloske, B. L. & Paranchych, W. Mutations in the fifth position glutamate in Pseudomonas aeruginosa pilin affect the transmethylation of the N-terminal phenylalanine. Can. J. Microbiol. 39, 500-505 (1993).
58. Forest, K. T. & Tainer, J. A. Type-4 pilus-structure: outside to inside and top to bottom - a minireview. Gene 192, 165-169 (1997).
59. Marceau, M., Forest, K., Beretti, J. L., Tainer, J. & Nassif, X. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol. Microbiol. 27, 705-715 (1998).
60. Forest, K. T., Dunham, S. A., Koomey, M. & Tainer, J. A. Crystallographic structure reveals phosphorylated pilin from Neisseria phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol. Microbiol. 31, 743-752 (1999).
61. Zhang, H. Z. & Donnenberg, M. S. DsbA is required for stability of the type IV of enteropathogenic Escherichia coli. Mol. Microbiol. 21, 787-797 (1996).
62. Kirn, T. J., Lafferty, M. J., Sandoe, C. M. & Taylor R. K. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35, 896-910 (2000).
63. Richardson, J. S. The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167-339 (1981).
64. Lee, K. K. et al. 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 (1994).
65. Krivan, H. C., Roberts, D. D. & Ginsburg, V. Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc β-1-4Gal found in some glycolipids. Proc. Natl Acad. Sci. USA 85, 6157-6161 (1986).
66. Ramphal, R., Sadoff, J. C., Pyle, M. & Silipigni, J. D. Role of pili in the adherence of Pseudomonas aeruginosa to injured tracheal epithelium. Infect. Immun. 44, 38-40 (1984).
67. Sun, D., Seyer, J. M., Kovari, I. Siumrada, R. A. & Taylor, R. K. Localization of protective epitopes within the pilin subunit of the Vibrio cholerae toxin-coregulated pilus. Infect. Immun. 59 114-118 (1991).
68. Virji, M. & Heckels, J. E. The role of common and type-specific pilus antigenic domains in adhesion and virulence of gonococci for human epithelial cells. J. Gen. Microbiol. 130, 1089-1095 (1984).
69. Forest, K. T. et al. Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies. Infect. Immun. 64, 644-652 (1996).
70. Watts, T. H., Kay, C. M. & Paranchych, W. Dissociation and characterization of pilin isolated from Pseudomonas aeruginosa strains PAK and PAO. Can. J. Biochem. 60, 867-872 (1982).
71. Watts, T. H., Kay, C. M. & Paranchych, W. Spectral properties of three quaternary arrangements of Pseudomonas pilin. Biochemistry 22, 3640-3646 (1983).
72. Bayley, D. P. & Jarrell, K. F. Further evidence to suggest that archaeal flagella are related to bacteria] type IV pili. J. Mol. Evol. 46, 370-373 (1998).
73. Cohen-Krausz, S. & Trachtenberg, S. The structure of the archeabacterial flagellar filament of the extreme halophile Halobacterium salinarum R1M1 and its relation to eubacterial flagellar filaments and type IV pili. J. Mol. Biol. 321, 383-395 (2002).
74. Bardy, S. L., Ng, S. Y. & Jarrell, K. F. Prokaryotic, motility structures. Microbiology 149, 295-304 (2003).
75. Correia, J. D. & Jarrell, K. F. Posttranslational processing of Methanococcus voltae preflagellin by preflagellin peptidases of M. voltae and other methanogens. J. Bacteriol. 182, 855-858 (2000).
76. Peabody, C. R. et al. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149, 3051-3072 (2003).
77. Nunn, D. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9, 402-408 (1999).
78. Sandkvist, M. Biology of type II secretion. Mol. Microbiol. 40, 271-283 (2001).
79. Sandkvist, M. Type II secretion and pathogenesis. Infect. Immun. 69, 3523-3535 (2001).
80. Sauvonnet, N., Vignon, G., Pugsley, A. P. & Gounon, P. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19, 2221-2228 (2000).
81. Vignon, G. et al. Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides. J. Bacteriol. 185, 3416-3428 (2003).
82. Durand, E. et al. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185, 2749-2758 (2003).
83. Tsui, I. S., Yip, C. M., Hackett, J. & Morris, C. The type IVB pili of Salmonella enterica serovar Typhi bind to the cystic fibrosis transmembrane conductance regulator. Infect. Immun. 71 6049-6050 (2003).
84. Tobe, T. & Sasakawa, C. Role of bundle-forming pilus of enteropathogenic Escherichia coli in host cell adherence and in microcolony development. Cell. Microbiol. 3, 579-585 (2001 ).
85. Tobe, T. & Sasakawa, C. Species-specific cell adhesion of enteropathogenic Escherichia coli is mediated by type IV bundle-forming pili. Cell. Microbiol. 4, 29-42 (2002).
86. Doig, P. et al. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect. Immun. 56, 1641-1646 (1988).
87. Krivan, H. C., Ginsburg, V. & Roberts, D. D. Pseudomonas aeruginosa and Pseudomonas cepacia isolated from cystic fibrosis patients bind specifically to gangliotetraosylceramide (asialo GM1) and gangliotraosylceramide (asialo GM2). Arch. Biochem. Biophys. 260 493-496 (1988).
88. Ramphal, R. et al. Pseudomonas aeruginosa recognizes carbohydrate chains containing type 1 (Gal β-1-3GlcNAc) or type 2 (Gal β-1-4GlcNAc) disaccharde units. Infect. Immun. 59, 700-704 (1991).
89. Doig, P., Paranchych, W., Sastry, P. A. & Irvin, R. T. Human buccal epithelial cell receptors of Pseudomonas aeruginosa: identification of glycoproteins with pilus binding activity. Can. J. Microbiol. 35, 1141-1145 (1989).
90. Lee, K. K., Doig, P., Irvin, R. T., Paranchych, W. & Hodges, R. S. Mapping the surface regions of Pseudomonas aeruginosa PAK pilin: the importance of the C-terminal region for adherence to human buccal epithelial cells. Mol. Microbiol. 3, 1493-1499 (1989).
91. Doig, P. et al. Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies directed against pili. Infect. Immun. 58 124-130 (1990).
92. Farinha, M. A. et al. Alteraticin of the pilin adhesion of Pseudomonas aeruginosa PAO results in normal pilus biogenesis but a loss of adherence to human pneumocyte cells and decreased virulence in mice. Infect. Immun. 62, 4118-4123 (1994).
93. Wong, W. Y. et al. Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa strains PAK and KB7. Biochemistry 34, 12963-12972 (1995).
94. Sheth, H. B. et al. Development of an anti-adhesion vaccine for Pseudomonas aeruginosa targeting the C-terminal region of the pilin structural protein. Biomed. Pept. Proteins Nucleic Acids 1, 141-148 (1995).
95. Lepper A. W., Moore, L. J., Atwell, J. L. & Tennent, J. M. The protective efficacy of pili from different strains of Moraxella bovis within the same serogroup against infectious bovine keratoconjunctivitis. Vet. Microbiol. 32, 177-187 (1992).
96. Hunt, J. D., Jackson, D. C. Brown, L. E., Woody, P. R. & Stewart, D. J. Antigenic competition in a multivalent foot rot vaccine. Vaccine 12, 457-464 (1994).
97. Egerton, J. R. et al. Protection of sheep against footrot with a recombinant DNA-based fimbrial vaccine. Vet. Microbiol. 14, 393-409 (1987).
98. Swanson, J., Robbins, K., Barrera, O. & Koomey, J. M. Gene conversion variations generate structurally distinct pilin polypeptides in Neisseria gonorrhoeae. J. Exp. Med. 165, 1016-1025 (1987).
99. Kellogg, D. S. Jr, Cohen, I. R., Norins, L. C., Schroeter, A. L. & Reising, G. Neisseria gonorrhoeae. II. Colonial variation and pathogenicity during 35 months in vitro. J. Bacteriol. 96, 596-605 (1968).
100. Kallstrom, H., Liszewski, M. K., Atkinson, J. P. & Jonsson, A. B. Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol. Microbiol. 25, 639-647 (1997).
101. Liszewski, M. K., Post, T. W. & Atkinson, J. P. Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu. Rev. Immunol. 9, 431-455 (1991).
102. Haas, R., Schwarz, H. & Meyer, T. F. Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc. Natl Acad. Sci. USA 84, 9079-9083 (1987).
103. Rytkonen, A., Johansson, L., Asp, V., Albiger, B. & Jonsson, A. B. Soluble pilin of Neisseria gonorrhoeae interacts with human target cells and tissue. Infect. Immun. 69, 6419-6426 (2001).
104. Rudel, T., van Putten, J. P., Gibbs, C. P., Haas, R. & Meyer, T. F. Interaction of two variable proteins (PilE and pilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol. Microbiol. 6, 3439-3450 (1992).
105. Scheuerpflug, I., Rudel, T., Ryll, R., Pandit, J. & Meyer, T. F. Roles of PilC and PilE proteins in pilus-mediated adherence of Neisseria gonorrhoeae and Neisseria meningitidis to human erythrocytes and endothelial and epithelial cells. Infect. Immun. 67, 834-843 (1999).
106. Nassif, X. et al. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc. Natl Acad. Sci. USA 91, 3769-3773 (1994).
107. Rudel, T., Scheurerpflug, I. & Meyer, T. F. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373, 357-359 (1995).
108. Jonsson, A. B., Ilver, D., Falk, P., Pepose, J. & Normark, S. Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 13, 403-416 (1994).
109. Jonsson, A. B., Nyberg, G. & Normark, S. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10, 477-488 (1991).
110. Winther-Larsen, H. C. et al. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl Acad. Sci. USA 98, 15276-15281 (2001).
111. Hagblom, P., Segal, E., Billyard, E. & So, M. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315, 156-158 (1985).
112. Segal, E., Billyard, E., So, M., Storzbach, S. & Meyer, T. F. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40, 293-300 (1985).
113. Long, C. D., Madraswala, R. N. & Seifert, H. S. Comparisons between colony phase variation of Neisseria gonorrhoeae FA1090 and pilus, pilin, and S-pilin expression. Infect. Immun. 66, 1918-1927 (1998).
114. Stern, A., Nickel, P., Meyer, T. F. & So, M. Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonococcal pilus gene. Cell 37, 447-456 (1984).
115. Boslego, J. W. et al. Efficacy trial of a parenteral gonococcal pilus vaccine in men. Vaccine 9, 154-162 (1991).
116. Rytkonen, A. et al. Neisseria meningitidis undergoes PilC phase variation and PilE sequence variation during invasive disease. J. Infect. Dis. 189, 402-409 (2004).
117. Comer, J. E., Marshall, M. A., Blanch, V. J., Deal, C. D. & Castric, P. Identification of the Pseudomonas aeruginosa 1244 pilin glycosylation site. Infect. Immun. 70, 2837-2845 (2002).
118. Castric, P., Cassels, F. J. & Carson, R. W. Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276, 26479-26485 (2001).
119. Kaiser, D. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 76, 5952-5956 (1979).
120. Sun, H., Zusman, D. R. & Shi, W. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10, 1143-1146 (2000).
121. Skerker, J. M. & Berg, H. C. Direct observation of extension and retraction of type IV pili. Proc. Natl Acad. Sci. USA 98, 6901-6904 (2001).
122. Whitchurch, C. B., Hobbs, M., Livingston, S. P., Krishnapillai, V. & Mattick, J. S. Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. Gene 101, 33-44 (1991).
123. Wolfgang, M., van Putten, J. P., Hayes, S. F., Dorward, D. & Koomey, M, Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 19, 6408-6418 (2000).
124. Kaiser, D. Bacterial motility: how do pili pull? Curr. Biol. 10, R777-R780 (2000).
125. Fussenegger, M., Rudel, T., Barten, R., Ryll, R. & Meyer, T. F. Transformation competence and type-4 pilus biogenesis in Nesseria gonorrhoeae - a review. Gene 192, 125-134 (1997).
126. Vuopio-Varkila, J. & Schoolnik, G. K. 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 (1991).
127. Cravioto, A., Gross, R. J., Scotland S. M. & Rowe, B. An adhesive factor found in strains of Escherichia coli belonging to the tradiitional infantile enteropathogenic serotypes. Curr. Microbiol. 3, 95-99 (1979).
128. Scaletsky, I. C., Silva, M. L. & Trabulsi, L. R. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect. Immun. 45, 534-536 (1984).
129. Hicks, S., Frankel, G., Kaper, J. B., Dougan, G. & Phillips, A. D. Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect. Immun. 66, 1570-1578 (1998).
130. Donnenberg, M. S., Kaper, J. B. & Finlay, B. B. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5, 109-114 (1997).
131. Nataro, J. P. et al. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6, 829-831 (1987).
132. Knutton, S., Shaw, R. K., Anantha, R. P., Donnenberg, M. S. & Zorgani, A. A. The type IV bundle-forming pilus of enteropathogenic Escherichia coli undergoes dramatic alterations in structure associated with bacterial adherence, aggregation and dispersal. Mol. Microbiol. 33, 499-509 (1999).
133. O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295-304 (1998).
134. Klausen, M., Aaes-Jorgensen, A., Molin, S. & Tolker-Nielsen, T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50, 61-68 (2003).
135. Freitag, N. E., Seifert, H. S. & Koomey, M. Characterization of the pilF-pilD pilus-assembly locus of Neisseria gonorrhoeae. Mol. Microbiol. 16, 575-586 (1995).
136. Tonjum, T., Freitag, N. E., Namork, E. & Koomey, M. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol. Microbiol. 16 451-464 (1995).
137. Drake, S. L. & Koomey, M. The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol. Microbiol. 18, 975-986 (1995).
138. Aas, F. E. et al. Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol. Microbiol. 46, 749-760 (2002).
139. Karaolis, D. K., Somara, S., Maneval, D. R. Jr, Johnson, J. A. & Kaper, J. B. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399, 375-379 (1999).
140. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910-1914 (1996).
141. Bradley, D. A pilus-dependent Pseudomonas aeruginosa bacteriophage with a long noncontractile tail. Virology 51, 489-492 (1973).
142. Sun, T. P. & Webster, R. E. Nucleotide sequence of a gene cluster involved in entry of colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J. Bacteriol. 169, 2667-2674 (1987).
143. Novotny, C. P. & Fives-Taylor, P. Retraction of F pili. J. Bacteriol. 117, 1306-1311 (1974).
144. Jacobson, A. Role of F pili in the penetration of bacteriophage f1. J. Virol. 10, 835-843 (1972).
145. 2+ flux triggers lysosome exocytosis and increases the amount of Lamp1 accessible to Neisseria IgA1 protease. Cell. Microbiol. 3, 265-275 (2001).
146. Kallstrom, H. & Jonsson, A. B. Characterization of the region downstream of the pilus biogenesis gene pilC1 in Neisseria gonorrhoeae. Biochim. Biophys. Acta 1397, 137-140 (1998).
147. Jendrossek, V. et al. Apoptotic response of Chang cells to infection with Pseudomonas aeruginosa strains PAK and PAO-I: molecular ordering of the apoptosis signaling cascade and role of type IV pili. Infect. Immun. 71, 2665-2673 (2003).
148. Abul-Milh, M., Wu, Y., Lau, B., Lingwood, C. A. & Foster, D. B. Induction of epithelial cell death including apoptosis by enteropathogenic Escherichia coli expressing bundle-forming pili. Infect. Immun. 69, 7356-7364 (2001).
149. Gill, D. B., Koomey, M., Cannon, J. G. & Atkinson, J. P. Down-regulation of CD46 by piliated Neisseria gonorrhoeae. J. Exp. Med. 198, 1313-1322 (2003).
150. Blom, A. M. et al. A novel interaction between type IV pili of Neisseria gonorrhoeae and the human complement regulator C4B-binding protein. J. Immunol. 166, 6764-6770 (2001).