Type IV pilus structure and bacterial pathogenicity (original) (raw)

• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Bieber, D. et al. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280, 2114–2118 (1998).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Merz, A. J., So, M. & Sheetz, M. P. Pilus retraction powers bacterial twitching motility. Nature 407, 98–102 (2000). The authors use laser tweezers to show that N. gonorrhoeae type IV pili tether the cells to a quartz surface and retract with a force that can exceed 80 pN, pulling cells forward, and that this process requires functional PilT.
  CAS PubMed Google Scholar
• Bragg, S. L. The Development of X-ray Analysis (eds Phillips, D. C. & Lipson, H.) (G. Bell, London, 1975).
  Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Robinson, R. C. et al. Domain movement in gelsolin: a calcium-activated switch. Science 286, 1939–1942 (1999).
  CAS PubMed Google Scholar
• Otterbein, L. R., Graceffa, P. & Dominguez, R. The crystal structure of uncomplexed actin in the ADP state. Science 293, 708–711 (2001).
  CAS Google Scholar
• Rayment, I. et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50–58 (1993).
  CAS PubMed Google Scholar
• Samatey, F. A. et al. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410, 331–337 (2001).
  CAS PubMed Google Scholar
• Sauer, F. G. et al. Structural basis of chaperone function and pilus biogenesis. Science 285, 1058–1061 (1999).
  CAS PubMed Google Scholar
• 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). Describes the first type IVb pilin structure for V. cholerae TcpA, which reveals a new protein fold, together with a full-length PAK pilin structure and a model for V. cholerae pilus assembly that is applicable to all type IV pili.
  CAS PubMed Google Scholar
• Parge, H. E. et al. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378, 32–38 (1995). The first structure of a type IV pilin reveals a ladle-shaped molecule with a 52-residue long N-terminal α-helix, an αβ-roll fold, a hypervariable β-hairpin and a covalently linked phosphate and disaccharide for GC pilin. A model for pilus assembly is presented based on symmetry of the PAK pilus filament.
  CAS PubMed Google Scholar
• 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). This first structure of the PAK pilin globular head domain reveals a similar fold to GC pilin and a receptor-binding loop that presents a surface dominated by main chain atoms.
  CAS PubMed Google Scholar
• 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). NMR solution structure of the soluble domain of P. aeruginosa K122-4 pilin showing an unusually large angle between the N-terminal α-helix and β-sheet compared with GC and PAK pilin. A model for K122-4 pilus assembly is also presented.
  CAS PubMed Google Scholar
• Yonekura, K., Maki-Yonekura, S. & Namba, K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424, 643–650 (2003).
  CAS PubMed Google Scholar
• Li, H., DeRosier, D., Nicholson, W., Nogales, E. & Downing, K. Microtubule structure at 8 Å resolution. Structure 10, 1317 (2002).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Pauling, L. & Corey, R. B. Two hydrogen-bonded spiral configurations of the polypeptide chain. J. Am. Chem. Soc. 72, 534 (1950).
  Google Scholar
• Franklin, R. & Gosling, R. G. Molecular configuration in sodium thymonucleate. Nature 171, 740–741 (1953).
  CAS PubMed Google Scholar
• Watson, J. D. & Crick, F. H. C. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737–738 (1953).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Bryan, R. K., Bansal, M., Folkhard, W., Nave, C. & Marvin, D. A. Maximum-entropy calculation of the electron density at 4 Å resolution of Pf1 filamentous bacteriophage. Proc. Natl Acad. Sci. USA 80, 4728–4731 (1983).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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). X-ray fibre diffraction data for GC and PAK pili indicate differences in their packing arrangements.
  Google Scholar
• Marvin, D. A. & Folkhard, W. Structure of F-pili: reassessment of the symmetry. J. Mol. Biol. 191, 299–300 (1986).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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). First X-ray fibre diffraction analysis of PAK and PAO pili defining their helical symmetry.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Potts, W. J. & Saunders, J. R. Nucleotide sequence of the structural gene for class I pilin from Neisseria meningitidis: homologies with the pilE locus of Neisseria gonorrhoeae. Mol. Microbiol. 2, 647–653 (1988).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Bradley, D. E. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can. J. Microbiol. 26, 146–154 (1980).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Marrs, C. F. et al. Cloning and sequencing of a Moraxella bovis pilin gene. J. Bacteriol. 163, 132–139 (1985).
  CAS PubMed PubMed Central Google Scholar
• Tonjum, T., Marrs, C. F., Rozsa, F. & Bovre, K. The type 4 pilin of Moraxella nonliquefaciens exhibits unique similarities with the pilins of Neisseria gonorrhoeae and Dichelobacter (Bacteroides) nodosus. J. Gen. Microbiol. 137, 2483–2490 (1991).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Rendulic, S. et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303, 689–692 (2004).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Giron, J. A., Ho, A. S. & Schoolnik, G. K. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254, 710–713 (1991).
  CAS PubMed Google Scholar
• Taniguchi, T., Fujino, Y., Yamamoto, K., Miwatani, T. & Honda, T. 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 (1995).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Forest, K. T. & Tainer, J. A. Type-4 pilus-structure: outside to inside and top to bottom — a minireview. Gene 192, 165–169 (1997).
  CAS PubMed Google Scholar
• 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). The authors identify the MC pilin glycosylation site at Ser63 and show that glycosylation does not have an important role in pilus assembly or adhesion but is required for expression of S pilin.
  CAS PubMed Google Scholar
• 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). The covalently linked phosphate at Ser63 of GC pilin was removed by mutation (Ser to Ala), producing pili that were functionally indistinguishable from the wild type in vitro , but were less straight and more bundled, indicating that the phosphate might have a minor role in pilus assembly.
  CAS PubMed Google Scholar
• Zhang, H. Z. & Donnenberg, M. S. DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol. Microbiol. 21, 787–797 (1996).
  CAS PubMed Google Scholar
• 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). Discrete functional domains are identified in the D-region of V. cholerae TcpA. The first two-thirds of the D-region are required for pilin folding and/or pilus assembly and are predicted to be buried in the TCP filament, and the last third of the D-region is involved in pilus–pilus interactions and predicted to be surface-exposed.
  CAS PubMed Google Scholar
• Richardson, J. S. The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167–339 (1981).
  CAS PubMed Google Scholar
• 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). The authors present strong evidence that the receptor-binding region of PAK pilin is buried along the length of the pilus filament and only exposed at its tip.
  CAS PubMed Google Scholar
• 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 (1988).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Forest, K. T. et al. Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies. Infect. Immun. 64, 644–652 (1996).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Watts, T. H., Kay, C. M. & Paranchych, W. Spectral properties of three quaternary arrangements of Pseudomonas pilin. Biochemistry 22, 3640–3646 (1983).
  CAS PubMed Google Scholar
• Bayley, D. P. & Jarrell, K. F. Further evidence to suggest that archaeal flagella are related to bacterial type IV pili. J. Mol. Evol. 46, 370–373 (1998).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Bardy, S. L., Ng, S. Y. & Jarrell, K. F. Prokaryotic motility structures. Microbiology 149, 295–304 (2003).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Nunn, D. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9, 402–408 (1999).
  CAS PubMed Google Scholar
• Sandkvist, M. Biology of type II secretion. Mol. Microbiol. 40, 271–283 (2001).
  CAS PubMed Google Scholar
• Sandkvist, M. Type II secretion and pathogenesis. Infect. Immun. 69, 3523–3535 (2001).
  CAS PubMed PubMed Central Google Scholar
• 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). First demonstration that pseudopilins can form pilus-like 'pseudo-pili', achieved by overexpressing the 15 genes encoding the Klebsiella oxytoca pullulanase type II secreton in E. coli . This secreton also assembled the type IV pilin PpdD into pilus filaments.
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Doig, P. et al. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect. Immun. 56, 1641–1646 (1988).
  CAS PubMed PubMed Central Google Scholar
• 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 gangliotriaosylceramide (asialo GM2). Arch. Biochem. Biophys. 260, 493–496 (1988).
  CAS PubMed Google Scholar
• Ramphal, R. et al. Pseudomonas aeruginosa recognizes carbohydrate chains containing type 1 (Gal β-1–3GlcNAc) or type 2 (Gal β-1–4GlcNAc) disaccharide units. Infect. Immun. 59, 700–704 (1991).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Farinha, M. A. et al. Alteration of the pilin adhesin 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Sheth, H. B. et al. Development of an anti-adhesive vaccine for Pseudomonas aeruginosa targeting the C-terminal region of the pilin structural protein. Biomed. Pept. Proteins Nucleic Acids 1, 141–148 (1995).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Hunt, J. D., Jackson, D. C., Brown, L. E., Wood, P. R. & Stewart, D. J. Antigenic competition in a multivalent foot rot vaccine. Vaccine 12, 457–464 (1994).
  CAS PubMed Google Scholar
• Egerton, J. R. et al. Protection of sheep against footrot with a recombinant DNA-based fimbrial vaccine. Vet. Microbiol. 14, 393–409 (1987).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  PubMed PubMed Central Google Scholar
• 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). Identified the cell surface receptor for N. gonorrhoeae and established a direct interaction between GC pili and CD46.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Rudel, T., Scheurerpflug, I. & Meyer, T. F. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373, 357–359 (1995). Showed that PilC is present at the ends of N. gonorrhoea type IV pili, and implicated this protein in adhesion by showing PilC-mediated inhibition of pilus-mediated attachment of N. gonorrhoeae and N. meningitidis to human epithelial cells.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Hagblom, P., Segal, E., Billyard, E. & So, M. Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315, 156–158 (1985). Identified constant and antigenically variable regions of N. gonorrhoeae type IV pilin and showed that during the course of a human gonococcal infection, N. gonorrhoeae variants give rise to new isolates expressing altered pili.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar
• Boslego, J. W. et al. Efficacy trial of a parenteral gonococcal pilus vaccine in men. Vaccine 9, 154–162 (1991).
  CAS PubMed Google Scholar
• Rytkonen, A. et al. Neisseria meningitidis undergoes PilC phase variation and PilE sequence variation during invasive disease. J. Infect. Dis. 189, 402–409 (2004).
  PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Castric, P., Cassels, F. J. & Carlson, R. W. Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276, 26479–26485 (2001).
  CAS PubMed Google Scholar
• Kaiser, D. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 76, 5952–5956 (1979).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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). A direct demonstration that twitching motility is driven by type IV pilus retraction. Total internal reflection microscopy was used to record extension and retraction of fluorescently labelled type IV pili at rates of 0.5 μm s −1 in P. aeruginosa , and showed that pilus retraction propelled cells forward.
  CAS PubMed Google Scholar
• 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). Identified the gene for PilT and established a genetic relationship between the type IV pili and the type II secretion system on the basis of homology of assembly components.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Kaiser, D. Bacterial motility: how do pili pull? Curr. Biol. 10, R777–R780 (2000).
  CAS PubMed Google Scholar
• Fussenegger, M., Rudel, T., Barten, R., Ryll, R. & Meyer, T. F. Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae — a review. Gene 192, 125–134 (1997).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Donnenberg, M. S., Kaper, J. B. & Finlay, B. B. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5, 109–114 (1997).
  CAS PubMed Google Scholar
• Nataro, J. P. et al. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6, 829–831 (1987).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295–304 (1998).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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). Demonstrated that DNA binding and uptake occur in two discrete steps, with DNA binding requiring type IV pili and ComP, and DNA uptake requiring functional PilT.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996). Identified the filamentous phage CTXφ, which carries the structural genes for cholera toxin, and showed that CTXφ uses the V. cholerae TCP as its receptor.
  CAS PubMed Google Scholar
• Bradley, D. A pilus-dependent Pseudomonas aeruginosa bacteriophage with a long noncontractile tail. Virology 51, 489–492 (1973).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• Novotny, C. P. & Fives-Taylor, P. Retraction of F pili. J. Bacteriol. 117, 1306–1311 (1974).
  CAS PubMed PubMed Central Google Scholar
• Jacobson, A. Role of F pili in the penetration of bacteriophage f1. J. Virol. 10, 835–843 (1972).
  CAS PubMed PubMed Central Google Scholar
• Ayala, B. P. et al. The pilus-induced Ca2+ flux triggers lysosome exocytosis and increases the amount of Lamp1 accessible to Neisseria IgA1 protease. Cell. Microbiol. 3, 265–275 (2001).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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).
  CAS PubMed Google Scholar