Surface organelles assembled by secretion systems of Gram-negative bacteria: Diversity in structure and function

FEMS Microbiology Reviews

Volumn 36, Issue 6, 2012, Pages 1046-1082

  Thanassi, David G ^a   Bliska, James B ^a   Christie, Peter J ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Chaperone usher pathway; Fimbriae; Pili; Type III secretion; Type IV pili; Type IV secretion

Indexed keywords

BACTERIAL ENZYME; CHAPERONE; NEUTRALIZING ANTIBODY;

BACTERIAL CELL; BACTERIAL VIRULENCE; BACTERIUM PILUS; CELL ADHESION; CELL FUNCTION; CELL ORGANELLE; CELL STRUCTURE; CELL SURFACE; CYTOPLASM; GRAM NEGATIVE BACTERIUM; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; MICROBIAL DIVERSITY; NEISSERIA MENINGITIDIS; NONHUMAN; RECEPTOR BINDING; REVIEW; TWITCHING MOTILITY; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; FIMBRIAE, BACTERIAL; GRAM-NEGATIVE BACTERIA; MOLECULAR CHAPERONES; ORGANELLES; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84866938204     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2012.00342.x     Document Type: Review

References (350)

1. Aas FE, Lovold C & Koomey M (2002) An inhibitor of DNA binding and uptake events dictates the proficiency of genetic transformation in Neisseria gonorrhoeae: mechanism of action and links to Type IV pilus expression. Mol Microbiol 46: 1441-1450.
2. Abraham SN, Sun D, Dale JB & Beachey EH (1988) Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobactericeae. Nature 336: 682-684.
3. Akeda Y & Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911-915.
4. Akopyan K, Edgren T, Wang-Edgren H, Rosqvist R, Fahlgren A, Wolf-Watz H & Fallman M (2011) Translocation of surface-localized effectors in type III secretion. P Natl Acad Sci USA 108: 1639-1644.
5. Alvarez-Martinez CE & Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
6. Aly KA & Baron C (2007) The VirB5 protein localizes to the T-pilus tips in Agrobacterium tumefaciens. Microbiology 153: 3766-3775.
7. Aly KA, Krall L, Lottspeich F & Baron C (2008) The type IV secretion system component VirB5 binds to the trans-zeatin biosynthetic enzyme Tzs and enables its translocation to the cell surface of Agrobacterium tumefaciens. J Bacteriol 190: 1595-1604.
8. Anantha RP, McVeigh AL, Lee LH et al. (2004) Evolutionary and functional relationships of colonization factor antigen i and other class 5 adhesive fimbriae of enterotoxigenic Escherichia coli. Infect Immun 72: 7190-7201.
9. Anderson LB, Hertzel AV & Das A (1996) Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. P Natl Acad Sci USA 93: 8889-8894.
10. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J & Hultgren SJ (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105-107.
11. Anderson KL, Billington J, Pettigrew D et al. (2004) An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol Cell 15: 647-657.
12. Andrews GP, Strachan ST, Benner GE et al. (1999) Protective efficacy of recombinant Yersinia outer proteins against bubonic plague caused by encapsulated and nonencapsulated Yersinia pestis. Infect Immun 67: 1533-1537.
13. Aprikian P, Interlandi G, Kidd BA et al. (2011) The bacterial fimbrial tip acts as a mechanical force sensor. PLoS Biol 9: e1000617.
14. Arts J, van Boxtel R, Filloux A, Tommassen J & Koster M (2007) Export of the pseudopilin XcpT of the Pseudomonas aeruginosa type II secretion system via the signal recognition particle-Sec pathway. J Bacteriol 189: 2069-2076.
15. Atmakuri K, Ding Z & Christie PJ (2003) VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol Microbiol 49: 1699-1713.
16. Atmakuri K, Cascales E & Christie PJ (2004) Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54: 1199-1211.
17. Audette GF, Manchak J, Beatty P, Klimke WA & Frost LS (2007) Entry exclusion in F-like plasmids requires intact TraG in the donor that recognizes its cognate TraS in the recipient. Microbiology 153: 442-451.
18. Ayers M, Howell PL & Burrows LL (2010) Architecture of the type II secretion and type IV pilus machineries. Future Microbiol 5: 1203-1218.
19. Backert S (2000) Strand switching during rolling circle replication of plasmid-like DNA circles in the mitochondria of the higher plant Chenopodium album (L.). Plasmid 43: 166-170.
20. Backert S & Clyne M (2011) Pathogenesis of Helicobacter pylori infection. Helicobacter 16(Suppl 1): 19-25.
21. Backert S, Fronzes R & Waksman G (2008) VirB2 and VirB5 proteins: specialized adhesins in bacterial type-IV secretion systems? Trends Microbiol 16: 409-413.
22. Baga M, Norgren M & Normark S (1987) Biogenesis of E. coli Pap pili: PapH, a minor pilin subunit involved in cell anchoring and length modulation. Cell 49: 241-251.
23. Bailey S, Ward D, Middleton R, Grossmann JG & Zambryski PC (2006) Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interaction sites. P Natl Acad Sci USA 103: 2582-2587.
24. Banta LM, Kerr JE, Cascales E et al. (2011) An Agrobacterium VirB10 mutation conferring a type IV secretion system gating defect. J Bacteriol 193: 2566-2574.
25. Baron C & Coombes B (2007) Targeting bacterial secretion systems: benefits of disarmament in the microcosm. Infect Disord Drug Targets 7: 19-27.
26. Baron C, Thorstenson YR & Zambryski PC (1997) The lipoprotein VirB7 interacts with VirB9 in the membranes of Agrobacterium tumefaciens. J Bacteriol 179: 1211-1218.
27. Bayliss R, Harris R, Coutte L et al. (2007) NMR structure of a complex between the VirB9/VirB7 interaction domains of the pKM101 type IV secretion system. P Natl Acad Sci USA 104: 1673-1678.
28. Biais N, Ladoux B, Higashi D, So M & Sheetz M (2008) Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biol 6: e87.
29. Bieber D, Ramer SW, Wu C-Y, Murray WJ, Tobe T, Fernandez R & Schoolnik GK (1998) Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Eschichia coli. Science 208: 2114-2118.
30. Bitter W, Koster M, Latijnhouwers M, de Cock H & 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.
31. Blocker A, Komoriya K & Aizawa S (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. P Natl Acad Sci USA 100: 3027-3030.
32. Blocker AJ, Deane JE, Veenendaal AK, Roversi P, Hodgkinson JL, Johnson S & Lea SM (2008) What's the point of the type III secretion system needle? P Natl Acad Sci USA 105: 6507-6513.
33. Blomfield IC (2001) The regulation of pap and type 1 fimbriation in Escherichia coli. Adv Microb Physiol 45: 1-49.
34. Bock K, Breimer ME, Brignole A et al. (1985) Specificity of binding of a strain of uropathogenic Escherichia coli to Gala(1-4)Gal-containing glycosphingolipids. J Biol Chem 260: 8545-8551.
35. Brinton CC (1959) Non-flagellar appendages of bacteria. Nature 183: 782-786.
36. Broz P, Mueller CA, Muller SA, Philippsen A, Sorg I, Engel A & Cornelis GR (2007) Function and molecular architecture of the Yersinia injectisome tip complex. Mol Microbiol 65: 1311-1320.
37. Brubaker RR (2003) Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen). Infect Immun 71: 3673-3681.
38. Bullitt E & Makowski L (1995) Structural polymorphism of bacterial adhesion pili. Nature 373: 164-167.
39. Burrows LL (2005) Weapons of mass retraction. Mol Microbiol 57: 878-888.
40. Burrows TW & Bacon GA (1956) The basis of virulence in Pasteurella pestis: an antigen determining virulence. Br J Exp Pathol 37: 481-493.
41. Buts L, Bouckaert J, De Genst E et al. (2003) The fimbrial adhesin F17-G of enterotoxigenic Escherichia coli has an immunoglobulin-like lectin domain that binds N-acetylglucosamine. Mol Microbiol 49: 705-715.
42. Campos M, Francetic O & Nilges M (2011) Modeling pilus structures from sparse data. J Struct Biol 173: 436-444.
43. Carbonnelle E, Helaine S, Nassif X & Pelicic V (2006) A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 61: 1510-1522.
44. Cascales E & Christie PJ (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1: 137-150.
45. Cascales E & Christie PJ (2004a) Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. P Natl Acad Sci USA 101: 17228-17233.
46. Cascales E & Christie PJ (2004b) Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304: 1170-1173.
47. Castric P, Cassels FJ & Carlson RW (2001) Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J Biol Chem 276: 26479-26485.
48. Cegelski L, Marshall GR, Eldridge GR & Hultgren SJ (2008) The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 6: 17-27.
49. Cehovin A, Kroll JS & Pelicic V (2011) Testing the vaccine potential of PilV, PilX and ComP, minor subunits of Neisseria meningitidis type IV pili. Vaccine 29: 6858-6865.
50. Chamot-Rooke J, Mikaty G, Malosse C et al. (2011) Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331: 778-782.
51. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J & Waksman G (2009) Structure of the outer membrane complex of a type IV secretion system. Nature 462: 1011-1015.
52. Chen TH & Elberg SS (1977) Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect Immun 15: 972-977.
53. Chen SL, Hung CS, Pinkner JS et al. (2009) Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. P Natl Acad Sci USA 106: 22439-22444.
54. Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ & Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285: 1061-1066.
55. Christie PJ (2004) Bacterial type IV secretion: the Agrobacterium VirB/D4 and related conjugation systems. Biochim Biophys Acta 1694: 219-234.
56. Christie PJ (2009) Structural biology: translocation chamber's secrets. Nature 462: 992-994.
57. Cisneros DA, Bond PJ, Pugsley AP, Campos M & Francetic O (2011) Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation. EMBO J 31: 1041-1053.
58. Clarke M, Maddera L, Harris RL & Silverman PM (2008) F-pili dynamics by live-cell imaging. P Natl Acad Sci USA 105: 17978-17981.
59. Collins RF, Frye SA, Kitmitto A, Ford RC, Tonjum T & Derrick JP (2004) Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 A resolution. J Biol Chem 279: 39750-39756.
60. Comer JE, Marshall MA, Blanch VJ, Deal CD & Castric P (2002) Identification of the Pseudomonas aeruginosa 1244 pilin glycosylation site. Infect Immun 70: 2837-2845.
61. Comolli JC, Hauser AR, Waite L, Whitchurch CB, Mattick JS & Engel JN (1999) Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect Immun 67: 3625-3630.
62. Conradi J, Huber S, Gaus K et al. (2011) Cyclic RGD peptides interfere with binding of the Helicobacter pylori protein CagL to integrins alpha(V)beta (3) and alpha (5)beta (1). Amino Acids DOI:10.1007/s00726-011-1066-0.
63. Cordes FS, Komoriya K, Larquet E, Yang S, Egelman EH, Blocker A & Lea SM (2003) Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem 278: 17103-17107.
64. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
65. Cornelis GR, Agrain C & Sorg I (2006) Length control of extended protein structures in bacteria and bacteriophages. Curr Opin Microbiol 9: 201-206.
66. Coureuil M, Mikaty G, Miller F et al. (2009) Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325: 83-87.
67. Coureuil M, Lecuyer H, Scott MG et al. (2010) Meningococcus Hijacks a beta2-adrenoceptor/beta-Arrestin pathway to cross brain microvasculature endothelium. Cell 143: 1149-1160.
68. Cowan C, Philipovskiy AV, Wulff-Strobel CR, Ye Z & Straley SC (2005) Anti-LcrV antibody inhibits delivery of Yops by Yersinia pestis KIM5 by directly promoting phagocytosis. Infect Immun 73: 6127-6137.
69. Craig L & Li J (2008) Type IV pili: paradoxes in form and function. Curr Opin Struct Biol 18: 267-277.
70. Craig L, Taylor RK, Pique ME et al. (2003) 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.
71. Craig L, Pique ME & Tainer JA (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2: 363-378.
72. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH & Tainer JA (2006) Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23: 651-662.
73. Crowther LJ, Anantha RP & Donnenberg MS (2004) The inner membrane subassembly of the enteropathogenic Escherichia coli bundle-forming pilus machine. Mol Microbiol 52: 67-79.
74. Davis AJ, Diaz DA & Mecsas J (2010) A dominant-negative needle mutant blocks type III secretion of early but not late substrates in Yersinia. Mol Microbiol 76: 236-259.
75. Deane JE, Roversi P, Cordes FS et al. (2006) Molecular model of a type III secretion system needle: implications for host-cell sensing. P Natl Acad Sci USA 103: 12529-12533.
76. Deane JE, Abrusci P, Johnson S & Lea SM (2010) Timing is everything: the regulation of type III secretion. Cell Mol Life Sci 67: 1065-1075.
77. Derewenda U, Mateja A, Devedjiev Y, Routzahn KM, Evdokimov AG, Derewenda ZS & Waugh DS (2004) The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure (Camb) 12: 301-306.
78. Desin TS, Mickael CS, Lam PK, Potter AA & Koster W (2010) Protection of epithelial cells from Salmonella enterica serovar Enteritidis invasion by antibodies against the SPI-1 type III secretion system. Can J Microbiol 56: 522-526.
79. Dickenson NE, Zhang L, Epler CR, Adam PR, Picking WL & Picking WD (2011) Conformational changes in IpaD from Shigella flexneri upon binding bile salts provide insight into the second step of type III secretion. Biochemistry 50: 172-180.
80. Dietrich M, Bartfeld S, Munke R, Lange C, Ogilvie LA, Friedrich A & Meyer TF (2011) Activation of NF-kappaB by Neisseria gonorrhoeae is associated with microcolony formation and type IV pilus retraction. Cell Microbiol 13: 1168-1182.
81. Dodson KW, Pinkner JS, Rose T, Magnusson G, Hultgren SJ & Waksman GJ (2001) Structural basis of the interaction of the pyelonephritic E. coli adhesin to Its human kidney receptor. Cell 105: 733-743.
82. Donnenberg M, Giron J, Nataro J & Kaper J (1992) A plasmid encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 6: 3427.
83. Dreiseikelmann B (1994) Translocation of DNA across bacterial membranes. Microbiol Rev 58: 293-316.
84. Driessen AJ & Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643-667.
85. Du Y, Rosqvist R & Forsberg A (2002) Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 70: 1453-1460.
86. Duguid JP, Smith IW, Dempster G & Edmunds PN (1955) Non-flagellar filamentous appendages ("fimbriae") and hemagglutinating activity in bacterium coli. J Pathol Bacteriol 70: 335-348.
87. Duguid JP, Anderson ES & Campbell I (1966) Fimbriae and adhesive properties in Salmonellae. J Pathol Bacteriol 92: 107-138.
88. Durand E, Bernadac A, Ball G, Lazdunski A, Sturgis JN & Filloux A (2003) Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J Bacteriol 185: 2749-2758.
89. Durand E, Waksman G & Receveur-Brechot V (2011) Structural insights into the membrane-extracted dimeric form of the ATPase TraB from the Escherichia coli pKM101 conjugation system. BMC Struct Biol 11: 4.
90. Eisele NA & Anderson DM (2009) Dual-function antibodies to Yersinia pestis LcrV required for pulmonary clearance of plague. Clin Vaccine Immunol 16: 1720-1727.
91. Eisenbrandt R, Kalkum M, Lai EM, Lurz R, Kado CI & Lanka E (1999) Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J Biol Chem 274: 22548-22555.
92. Enninga J & Rosenshine I (2009) Imaging the assembly, structure and activity of type III secretion systems. Cell Microbiol 11: 1462-1470.
93. Epler CR, Dickenson NE, Olive AJ, Picking WL & Picking WD (2009) Liposomes recruit IpaC to the Shigella flexneri type III secretion apparatus needle as a final step in secretion induction. Infect Immun 77: 2754-2761.
94. Erskine PT, Knight MJ, Ruaux A et al. (2006) High resolution structure of BipD: an invasion protein associated with the type III secretion system of Burkholderia pseudomallei. J Mol Biol 363: 125-136.
95. Espina M, Olive AJ, Kenjale R et al. (2006) IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect Immun 74: 4391-4400.
96. Eto DS, Jones TA, Sundsbak JL & Mulvey MA (2007) Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 3: e100.
97. Fallman E, Schedin S, Jass J, Uhlin BE & Axner O (2005) The unfolding of the P pili quaternary structure by stretching is reversible, not plastic. EMBO Rep 6: 52-56.
98. Felek S, Jeong JJ, Runco LM, Murray S, Thanassi D & Krukonis ES (2011) Contributions of chaperone/usher systems to cell binding, biofilm formation and Yersinia pestis virulence. Microbiology 157: 805-818.
99. Felise HB, Nguyen HV, Pfuetzner RA et al. (2008) An inhibitor of gram-negative bacterial virulence protein secretion. Cell Host Microbe 4: 325-336.
100. Fernandez D, Spudich GM, Zhou XR & Christie PJ (1996) The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol 178: 3168-3176.
101. Fields KA, Nilles ML, Cowan C & Straley SC (1999) Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun 67: 5395-5408.
102. Fischer W (2011) Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J 278: 1203-1212.
103. Forero M, Yakovenko O, Sokurenko EV, Thomas WE & Vogel V (2006) Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds. PLoS Biol 4: e298.
104. Francetic O, Buddelmeijer N, Lewenza S, Kumamoto CA & Pugsley AP (2007) Signal recognition particle-dependent inner membrane targeting of the PulG Pseudopilin component of a type II secretion system. J Bacteriol 189: 1783-1793.
105. Frank DW, Vallis A, Wiener-Kronish JP et al. (2002) Generation and characterization of a protective monoclonal antibody to Pseudomonas aeruginosa PcrV. J Infect Dis 186: 64-73.
106. Fronzes R, Christie PJ & Waksman G (2009a) The structural biology of type IV secretion systems. Nat Rev Microbiol 7: 703-714.
107. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV & Waksman G (2009b) Structure of a type IV secretion system core complex. Science 323: 266-268.
108. Frost LS & Koraimann G (2010) Regulation of bacterial conjugation: balancing opportunity with adversity. Future Microbiol 5: 1057-1071.
109. Fullner KJ, Lara JC & Nester EW (1996) Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273: 1107-1109.
110. Galan JE & Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567-573.
111. Galkin VE, Schmied WH, Schraidt O, Marlovits TC & Egelman EH (2010) The structure of the Salmonella typhimurium type III secretion system needle shows divergence from the flagellar system. J Mol Biol 396: 1392-1397.
112. Galyov EE, Smirnov O, Karlishev AV et al. (1990) Nucleotide sequence of the Yersinia pestis gene encoding F1 antigen and the primary structure of the protein. Putative T and B cell epitopes. FEBS Lett 277: 230-232.
113. Garmendia J, Frankel G & Crepin VF (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73: 2573-2585.
114. Gibiansky ML, Conrad JC, Jin F et al. (2010) Bacteria use type IV pili to walk upright and detach from surfaces. Science 330: 197.
115. Gil H, Benach JL & Thanassi DG (2004) Presence of pili on the surface of Francisella tularensis. Infect Immun 72: 3042-3047.
116. Giron JA, Ho ASY & Schoolnik GK (1991) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710-713.
117. Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, de la Cruz F & Coll M (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1- ATPase. Nature 409: 637-641.
118. Gomis-Ruth FX, de la Cruz F & Coll M (2002) Structure and role of coupling proteins in conjugal DNA transfer. Res Microbiol 153: 199-204.
119. Gomis-Ruth FX, Sola M, de la Cruz F & Coll M (2004) Coupling factors in macromolecular type-IV secretion machineries. Curr Pharm Des 10: 1551-1565.
120. Goure J, Broz P, Attree O, Cornelis GR & Attree I (2005) Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 192: 218-225.
121. Haas R & Meyer T (1986) The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44: 107-115.
122. Hager AJ, Bolton DL, Pelletier MR et al. (2006) Type IV pili-mediated secretion modulates Francisella virulence. Mol Microbiol 62: 227-237.
123. Hahn E, Wild P, Hermanns U et al. (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323: 845-857.
124. Han X, Kennan RM, Parker D, Davies JK & Rood JI (2007) Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus. J Bacteriol 189: 5022-5033.
125. Hansen JK & Forest KT (2006) Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. J Mol Microbiol Biotechnol 11: 192-207.
126. Hapfelmeier S, Domke N, Zambryski PC & Baron C (2000) VirB6 is required for stabilization of VirB5 and VirB3 and formation of VirB7 homodimers in Agrobacterium tumefaciens. J Bacteriol 182: 4505-4511.
127. Hare S, Bayliss R, Baron C & Waksman G (2006) A large domain swap in the VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J Mol Biol 360: 56-66.
128. Hayward RD, Cain RJ, McGhie EJ, Phillips N, Garner MJ & Koronakis V (2005) Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol Microbiol 56: 590-603.
129. Hazes B, Sastry PA, Hayakawa K, Read RJ & Irvin RT (2000) Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 299: 1005-1017.
130. Hegge FT, Hitchen PG, Aas FE et al. (2004) Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. P Natl Acad Sci USA 101: 10798-10803.
131. Heiniger RW, Winther-Larsen HC, Pickles RJ, Koomey M & Wolfgang MC (2010) Infection of human mucosal tissue by Pseudomonas aeruginosa requires sequential and mutually dependent virulence factors and a novel pilus-associated adhesin. Cell Microbiol 12: 1158-1173.
132. Helaine S, Carbonnelle E, Prouvensier L, Beretti JL, Nassif X & Pelicic V (2005) PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol 55: 65-77.
133. Helaine S, Dyer DH, Nassif X, Pelicic V & Forest KT (2007) 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. P Natl Acad Sci USA 104: 15888-15893.
134. Henderson NS, Ng TW, Talukder I & Thanassi DG (2011) Function of the usher N-terminus in catalysing pilus assembly. Mol Microbiol 79: 954-967.
135. Hill J, Leary SE, Griffin KF, Williamson ED & Titball RW (1997) Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization. Infect Immun 65: 4476-4482.
136. Hill J, Leary S, Smither S et al. (2009) N255 is a key residue for recognition by a monoclonal antibody which protects against Yersinia pestis infection. Vaccine 27: 7073-7079.
137. Hobbs M & Mattick JS (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.
138. Hoiczyk E & Blobel G (2001) Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. P Natl Acad Sci USA 98: 4669-4674.
139. Howell-Adams B & Seifert HS (1999) Insertion mutations in pilE differentially alter gonococcal pilin antigenic variation. J Bacteriol 181: 6133-6141.
140. Howie HL, Glogauer M & So M (2005) The N. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a pilT-dependent mechanism. PLoS Biol 3: e100.
141. Hume PJ, McGhie EJ, Hayward RD & Koronakis V (2003) The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol Microbiol 49: 425-439.
142. Hung DL, Knight SD, Woods RM, Pinkner JS & Hultgren SJ (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15: 3792-3805.
143. Hung CS, Bouckaert J, Hung D et al. (2002) Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol 44: 903-915.
144. Hyland RM, Sun J, Griener TP, Mulvey GL, Klassen JS, Donnenberg MS & Armstrong GD (2008) The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin. Cell Microbiol 10: 177-187.
145. Ivanov MI, Noel BL, Rampersaud R, Mena P, Benach JL & Bliska JB (2008) Vaccination of mice with a Yop translocon complex elicits antibodies that are protective against infection with F1- Yersinia pestis. Infect Immun 76: 5181-5190.
146. Jacob-Dubuisson F, Heuser J, Dodson K, Normark S & Hultgren SJ (1993) Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J 12: 837-847.
147. Jakubowski SJ, Krishnamoorthy V & Christie PJ (2003) Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J Bacteriol 185: 2867-2878.
148. Jakubowski SJ, Krishnamoorthy V, Cascales E & Christie PJ (2004) Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J Mol Biol 341: 961-977.
149. Jakubowski SJ, Cascales E, Krishnamoorthy V & Christie PJ (2005) Agrobacterium tumefaciens VirB9, an outer-membrane-associated component of a type IV secretion system, regulates substrate selection and T-pilus biogenesis. J Bacteriol 187: 3486-3495.
150. Jakubowski SJ, Kerr JE, Garza I, Krishnamoorthy V, Bayliss R, Waksman G & Christie PJ (2009) Agrobacterium VirB10 domain requirements for type IV secretion and T. pilus biogenesis. Mol Microbiol 71: 779-794.
151. Johansson L, Rytkonen A, Bergman P et al. (2003) CD46 in meningococcal disease. Science 301: 373-375.
152. Johnson S, Roversi P, Espina M et al. (2007) Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J Biol Chem 282: 4035-4044.
153. Jones CH, Pinkner JS, Roth R, Heuser J, Nicholoes AV, Abraham SN & Hultgren SJ (1995) FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. P Natl Acad Sci USA 92: 2081-2085.
154. Jude BA & Taylor RK (2011) The physical basis of type 4 pilus-mediated microcolony formation by Vibrio cholerae O1. J Struct Biol 175: 1-9.
155. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW & Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33: 376-393.
156. Justice SS, Hung C, Theriot JA, Fletcher DA, Anderson GG, Footer MJ & Hultgren SJ (2004) Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. P Natl Acad Sci USA 101: 1333-1338.
157. Kalkum M, Eisenbrandt R, Lurz R & Lanka E (2002) Tying rings for sex. Trends Microbiol 10: 382-387.
158. Kao DJ, Churchill ME, Irvin RT & Hodges RS (2007) Animal protection and structural studies of a consensus sequence vaccine targeting the receptor binding domain of the type IV pilus of Pseudomonas aeruginosa. J Mol Biol 374: 426-442.
159. Karnholz A, Hoefler C, Odenbreit S, Fischer W, Hofreuter D & Haas R (2006) Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J Bacteriol 188: 882-893.
160. Kenjale R, Wilson J, Zenk SF, Saurya S, Picking WL, Picking WD & Blocker A (2005) The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J Biol Chem 280: 42929-42937.
161. Kerr JE & Christie PJ (2010) Evidence for VirB4-mediated dislocation of membrane-integrated VirB2 pilin during biogenesis of the Agrobacterium VirB/VirD4 type IV secretion system. J Bacteriol 192: 4923-4934.
162. Keyser P, Elofsson M, Rosell S & Wolf-Watz H (2008) Virulence blockers as alternatives to antibiotics: type III secretion inhibitors against Gram-negative bacteria. J Intern Med 264: 17-29.
163. Kirchner M, Heuer D & Meyer TF (2005) CD46-independent binding of neisserial type IV pili and the major pilus adhesin, PilC, to human epithelial cells. Infect Immun 73: 3072-3082.
164. Kirn TJ, Lafferty MJ, Sandoe CM & Taylor RK (2000) Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 35: 896-910.
165. Kirn TJ, Bose N & Taylor RK (2003) Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol Microbiol 49: 81-92.
166. Knutton S, Rosenshine I, Pallen MJ et al. (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17: 2166-2176.
167. Korea CG, Badouraly R, Prevost MC, Ghigo JM & Beloin C (2010) Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 12: 1957-1977.
168. Korotkov KV, Pardon E, Steyaert J & Hol WG (2009) Crystal structure of the N-terminal domain of the secretin GspD from ETEC determined with the assistance of a nanobody. Structure 17: 255-265.
169. Korotkova N, Le Trong I, Samudrala R et al. (2006) Crystal structure and mutational analysis of the DaaE adhesin of Escherichia coli. J Biol Chem 281: 22367-22377.
170. Kubori T, Matsushima Y, Nakamura D et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605.
171. Kuehn MJ, Heuser J, Normark S & Hultgren SJ (1992) P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 356: 252-255.
172. Kwok T, Zabler D, Urman S et al. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.
173. Lafont F & van der Goot FG (2005) Oiling the key hole. Mol Microbiol 56: 575-577.
174. Lang S, Gruber K, Mihajlovic S et al. (2010) Molecular recognition determinants for type IV secretion of diverse families of conjugative relaxases. Mol Microbiol 78: 1539-1555.
175. Lang S, Gruber CJ, Redzej A, Raffl S, Zellnig G, Zangger K & Zechner E (2011) An activation domain of plasmid R1 TraI protein delineates stages of gene transfer initiation. Mol Microbiol 82: 1071-1085.
176. Langermann S, Möllby R, Burlein JE et al. (2000) Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherhichia coli. J Infect Dis 181: 774-778.
177. Lara-Tejero M & Galan JE (2009) Salmonella enterica serovar typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun 77: 2635-2642.
178. Lawley TD, Klimke WA, Gubbins MJ & Frost LS (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224: 1-15.
179. Le Trong I, Aprikian P, Kidd BA et al. (2010) Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell 141: 645-655.
180. Lee KK, Sheth HB, Wong WY et al. (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.
181. Lee PC, Stopford CM, Svenson AG & Rietsch A (2010) Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 75: 924-941.
182. Li YF, Poole S, Rasulova F, McVeigh AL, Savarino SJ & Xia D (2007) A receptor-binding site as revealed by the crystal structure of CfaE, the colonization factor antigen I fimbrial adhesin of enterotoxigenic Escherichia coli. J Biol Chem 282: 23970-23980.
183. Li J, Lim MS, Li S, Brock M, Pique ME, Woods VL Jr & Craig L (2008) Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure 16: 137-148.
184. Li Q, Ng TW, Dodson KW et al. (2010) The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili. Mol Microbiol 76: 159-172.
185. Lim MS, Ng D, Zong S, Arvai AS, Taylor RK, Tainer JA & Craig L (2010) Vibrio cholerae El Tor Tcpa crystal structure and mechanism for pilus-mediated microcolony formation. Mol Microbiol 77: 755-770.
186. Liu F, Chen H, Galvan EM, Lasaro MA & Schifferli DM (2006) Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect Immun 74: 5636-5644.
187. Llosa M, Roy C & Dehio C (2009) Bacterial type IV secretion systems in human disease. Mol Microbiol 73: 141-151.
188. Low D, Braaten B & van der Woude M (1996) Fimbriae. Escherichia coli and Salmonella; Cellular and Molecular Biology (Neidhardt FC, ed), pp. 146-157. ASM Press, Washington, DC.
189. Lu J & Frost LS (2005) Mutations in the C-terminal region of TraM provide evidence for in vivo TraM-TraD interactions during F-plasmid conjugation. J Bacteriol 187: 4767-4773.
190. Lu HM, Motley ST & 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.
191. Lu J, Wong JJ, Edwards RA, Manchak J, Frost LS & Glover JN (2008) Structural basis of specific TraD-TraM recognition during F plasmid-mediated bacterial conjugation. Mol Microbiol 70: 89-99.
192. Macdonald DL, Pasloske BL & Paranchych W (1993) Mutations in the fifth-position glutamate in Pseudomonas aeruginosa pilin affect the transmethylation of the N-terminal phenylalanine. Can J Microbiol 39: 500-505.
193. Macnab RM (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694: 207-217.
194. Maier B, Potter L, So M, Long CD, Seifert HS & Sheetz MP (2002) Single pilus motor forces exceed 100 pN. P Natl Acad Sci USA 99: 16012-16017.
195. Mairey E, Genovesio A, Donnadieu E et al. (2006) Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. J Exp Med 203: 1939-1950.
196. Manning PA (1997) The tcp gene cluster of Vibrio cholerae. Gene 192: 63-70.
197. Marceau M, Beretti JL & Nassif X (1995) High adhesiveness of encapsulated Neisseria meningitidis to epithelial cells is associated with the formation of bundles of pili. Mol Microbiol 17: 855-863.
198. Marlovits TC & Stebbins CE (2010) Type III secretion systems shape up as they ship out. Curr Opin Microbiol 13: 47-52.
199. Marrero J & Waldor MK (2007) Determinants of entry exclusion within Eex and TraG are cytoplasmic. J Bacteriol 189: 6469-6473.
200. Marrs CF, Schoolnik G, Koomey JM, Hardy J, Rothbard J & Falkow S (1985) Cloning and sequencing of a Moraxella bovis pilin gene. J Bacteriol 163: 132-139.
201. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS & Hultgren SJ (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803-2812.
202. Martinez-Argudo I & Blocker AJ (2010) The Shigella T3SS needle transmits a signal for MxiC release, which controls secretion of effectors. Mol Microbiol 78: 1365-1378.
203. Matson JS, Durick KA, Bradley DS & Nilles ML (2005) Immunization of mice with YscF provides protection from Yersinia pestis infections. BMC Microbiol 5: 38.
204. Mattei PJ, Faudry E, Job V, Izore T, Attree I & Dessen A (2011) Membrane targeting and pore formation by the type III secretion system translocon. FEBS J 278: 414-426.
205. Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56: 289-314.
206. Mattick JS, Whitchurch CB & Alm RA (1996) The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa-a review. Gene 179: 147-155.
207. McGhie EJ, Hume PJ, Hayward RD, Torres J & Koronakis V (2002) Topology of the Salmonella invasion protein SipB in a model bilayer. Mol Microbiol 44: 1309-1321.
208. Merckel MC, Tanskanen J, Edelman S, Westerlund-Wikstrom B, Korhonen TK & Goldman A (2003) The structural basis of receptor-binding by Escherichia coli associated with diarrhea and septicemia. J Mol Biol 331: 897-905.
209. Merz AJ & So M (2000) Interactions of pathogenic neisseriae with epithelial cell membranes. Annu Rev Cell Dev Biol 16: 423-457.
210. Merz AJ, Enns CA & So M (1999) Type IV pili of pathogenic Neisseriae elicit cortical plaque formation in epithelial cells. Mol Microbiol 32: 1316-1332.
211. Merz AJ, So M & Sheetz MP (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102.
212. Mikaty G, Soyer M, Mairey E et al. (2009) Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS Pathog 5: e1000314.
213. Miller J, Williamson ED, Lakey JH, Pearce MJ, Jones SM & Titball RW (1998) Macromolecular organisation of recombinant Yersinia pestis F1 antigen and the effect of structure on immunogenicity. FEMS Immunol Med Microbiol 21: 213-221.
214. Miller E, Garcia T, Hultgren S & Oberhauser AF (2006) The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys J 91: 3848-3856.
215. Mills JA, Buysse JM & Oaks EV (1988) Shigella flexneri invasion plasmid antigens B and C: epitope location and characterization with monoclonal antibodies. Infect Immun 56: 2933-2941.
216. Misic AM, Satyshur KA & Forest KT (2010) P. aeruginosa PilT structures with and without nucleotide reveal a dynamic type IV pilus retraction motor. J Mol Biol 400: 1011-1021.
217. Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B & Hardt WD (2011) Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun 79: 330-341.
218. Morand PC, Bille E, Morelle S et al. (2004) Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J 23: 2009-2017.
219. Mossey P, Hudacek A & Das A (2010) Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7, and VirB8 for stabilization. J Bacteriol 192: 2830-2838.
220. Mu XQ & Bullitt E (2006) Structure and assembly of P-pili: a protruding hinge region used for assembly of a bacterial adhesion filament. P Natl Acad Sci USA 103: 9861-9866.
221. Mueller CA, Broz P, Muller SA et al. (2005) The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310: 674-676.
222. Mueller CA, Broz P & Cornelis GR (2008) The type III secretion system tip complex and translocon. Mol Microbiol 68: 1085-1095.
223. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J & Hultgren SJ (1998) Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282: 1494-1497.
224. Mulvey MA, Schilling JD & Hultgren SJ (2001) Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69: 4572-4579.
225. Mysorekar IU & Hultgren SJ (2006) Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. P Natl Acad Sci USA 103: 14170-14175.
226. Nagai H & Kubori T (2011) Type IVB secretion systems of Legionella and other Gram-negative bacteria. Front Microbiol 2: 136.
227. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA & Roy CR (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. P Natl Acad Sci USA 102: 826-831.
228. Nakano N, Kubori T, Kinoshita M, Imada K & Nagai H (2010) Crystal structure of Legionella DotD: insights into the relationship between type IVB and type II/III secretion systems. PLoS Pathog 6: e1001129.
229. Nassif X, Beretti JL, Lowy J et al. (1994) Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. P Natl Acad Sci USA 91: 3769-3773.
230. Nishiyama M, Ishikawa T, Rechsteiner H & Glockshuber R (2008) Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320: 376-379.
231. Noel BL, Lilo S, Capurso D, Hill J & Bliska JB (2009) Yersinia pestis can bypass protective antibodies to LcrV and activation with gamma interferon to survive and induce apoptosis in murine macrophages. Clin Vaccine Immunol 16: 1457-1466.
232. Nuccio SP & Bäumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71: 551-575.
233. Nudleman E & Kaiser D (2004) Pulling together with type IV pili. J Mol Microbiol Biotechnol 7: 52-62.
234. O'Toole GA & Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
235. Olive AJ, Kenjale R, Espina M, Moore DS, Picking WL & Picking WD (2007) Bile salts stimulate recruitment of IpaB to the Shigella flexneri surface, where it colocalizes with IpaD at the tip of the type III secretion needle. Infect Immun 75: 2626-2629.
236. Orans J, Johnson MD, Coggan KA, Sperlazza JR, Heiniger RW, Wolfgang MC & Redinbo MR (2010) Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. P Natl Acad Sci USA 107: 1065-1070.
237. Orskov I & Orskov F (1990) Serologic classification of fimbriae. Curr Top Microbiol Immunol 151: 71-90.
238. Ottow JCG (1975) Ecology, physiology and genetics of fimbriae and pili. Annu Rev Microbiol 29: 79-108.
239. Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED & Tainer JA (1995) Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378: 32-38.
240. Pasloske BL, Scraba DG & Paranchych W (1989) Assembly of mutant pilins in Pseudomonas aeruginosa: formation of pili composed of heterologous subunits. J Bacteriol 171: 2142-2147.
241. Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP & Saier MH Jr (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149: 3051-3072.
242. Pelicic V (2008) Type IV pili: e pluribus unum? Mol Microbiol 68: 827-837.
243. Pettersson J, Holmstrom A, Hill J et al. (1999) The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 32: 961-976.
244. Pettigrew D, Anderson KL, Billington J et al. (2004) High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J Biol Chem 279: 46851-46857.
245. Phan G, Remaut H, Wang T et al. (2011) Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 474: 49-53.
246. Pinkner JS, Remaut H, Buelens F et al. (2006) Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. P Natl Acad Sci USA 103: 17897-17902.
247. Planet PJ, Kachlany SC, DeSalle R & Figurski DH (2001) Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. P Natl Acad Sci USA 98: 2503-2508.
248. Pohlschroder M, Ghosh A, Tripepi M & Albers SV (2011) Archaeal type IV pilus-like structures-evolutionarily conserved prokaryotic surface organelles. Curr Opin Microbiol 14: 357-363.
249. Poole ST, McVeigh AL, Anantha RP et al. (2007) Donor strand complementation governs intersubunit interaction of fimbriae of the alternate chaperone pathway. Mol Microbiol 63: 1372-1384.
250. Pratt LA & Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285-293.
251. Pron B, Taha MK, Rambaud C et al. (1997) Interaction of Neisseria maningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J Infect Dis 176: 1285-1292.
252. Pujol C, Eugene E, Marceau M & Nassif X (1999) The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. P Natl Acad Sci USA 96: 4017-4022.
253. Quenee LE, Berube BJ, Segal J, Elli D, Ciletti NA, Anderson D & Schneewind O (2010) Amino acid residues 196-225 of LcrV represent a plague protective epitope. Vaccine 28: 1870-1876.
254. Rakotoarivonina H, Jubelin G, Hebraud M, Gaillard-Martinie B, Forano E & Mosoni P (2002) Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148: 1871-1880.
255. Ramboarina S, Fernandes PJ, Daniell S et al. (2005) Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem 280: 40252-40260.
256. Ramsey ME, Woodhams KL & Dillard JP (2011) The gonococcal genetic island and type IV secretion in the pathogenic Neisseria. Front Microbiol 2: 61.
257. Reichow SL, Korotkov KV, Hol WG & Gonen T (2010) Structure of the cholera toxin secretion channel in its closed state. Nat Struct Mol Biol 17: 1226-1232.
258. Remaut H, Tang C, Henderson NS et al. (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133: 640-652.
259. Roberts JA, Marklund B-I, Ilver D et al. (1994) The Galα(1-4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. P Natl Acad Sci USA 91: 11889-11893.
260. Roehrich AD, Martinez-Argudo I, Johnson S, Blocker AJ & Veenendaal AK (2010) The extreme C terminus of Shigella flexneri IpaB is required for regulation of type III secretion, needle tip composition, and binding. Infect Immun 78: 1682-1691.
261. Rudel T, Scheuerpflug I & Meyer TF (1995a) Neisseria PilC protein identified as type 4 pilus tip-located adhesin. Nature 373: 357-359.
262. Rudel T, Boxberger HJ & Meyer TF (1995b) Pilus biogenesis and epithelial cell adherence of Neisseria gonorrhoeaepilC double knock-out mutants. Mol Microbiol 17: 1057-1071.
263. Runco LM, Myrczek S, Bliska JB & Thanassi DG (2008) Biogenesis of the fraction 1 capsule and analysis of the ultrastructure of Yersinia pestis. J Bacteriol 190: 3381-3385.
264. Sakellaris H & Scott JR (1998) New tools in an old trade: CS1 pilus morphogenesis. Mol Microbiol 30: 681-687.
265. Salminen A, Loimaranta V, Joosten JA, Khan AS, Hacker J, Pieters RJ & Finne J (2007) Inhibition of P-fimbriated Escherichia coli adhesion by multivalent galabiose derivatives studied by a live-bacteria application of surface plasmon resonance. J Antimicrob Chemother 60: 495-501.
266. Samuels AL, Lanka E & Davies JE (2000) Conjugative junctions in RP4-mediated mating of Escherichia coli. J Bacteriol 182: 2709-2715.
267. Sani M, Botteaux A, Parsot C, Sansonetti P, Boekema EJ & Allaoui A (2007) IpaD is localized at the tip of the Shigella flexneri type III secretion apparatus. Biochim Biophys Acta 1770: 307-311.
268. Sato H & Frank DW (2011) Multi-functional characteristics of the Pseudomonas aeruginosa type III needle-tip protein, PcrV; comparison to orthologs in other Gram-negative bacteria. Front Microbiol 2: 142.
269. Sato H, Hunt ML, Weiner JJ, Hansen AT & Frank DW (2011) Modified needle-tip PcrV proteins reveal distinct phenotypes relevant to the control of type III secretion and intoxication by Pseudomonas aeruginosa. PLoS ONE 6: e18356.
270. Satyshur KA, Worzalla GA, Meyer LS, Heiniger EK, Aukema KG, Misic AM & Forest KT (2007) Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 15: 363-376.
271. Sauer FG, Fütterer K, Pinkner JS, Dodson KW, Hultgren SJ & Waksman G (1999) Structural basis of chaperone function and pilus biogenesis. Science 285: 1058-1061.
272. Sauer FG, Pinkner JS, Waksman G & Hultgren SJ (2002) Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111: 543-551.
273. Sauvonnet N, Vignon G, Pugsley AP & Gounon P (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 19: 2221-2228.
274. Savvides SN (2007) Secretion superfamily ATPases swing big. Structure 15: 255-257.
275. Savvides SN, Yeo HJ, Beck MR et al. (2003) VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J 22: 1969-1980.
276. Sawa T, Yahr TL, Ohara M, Kurahashi K, Gropper MA, Wiener-Kronish JP & Frank DW (1999) Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat Med 5: 392-398.
277. Scheuerpflug I, Rudel T, Ryll R, Pandit J & Meyer TF (1999) 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.
278. Schroeder TH, Zaidi T & Pier GB (2001) Lack of adherence of clinical isolates of Pseudomonas aeruginosa to asialo-GM(1) on epithelial cells. Infect Immun 69: 719-729.
279. Schulein R, Guye P, Rhomberg TA et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. P Natl Acad Sci USA 102: 856-861.
280. Sebbane F, Jarrett C, Gardner D, Long D & Hinnebusch BJ (2009) The Yersinia pestis caf1M1A1 fimbrial capsule operon promotes transmission by flea bite in a mouse model of bubonic plague. Infect Immun 77: 1222-1229.
281. Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C & Abe A (2001) Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. P Natl Acad Sci USA 98: 11638-11643.
282. Shakhnovich EA, Hung DT, Pierson E, Lee K & Mekalanos JJ (2007) Virstatin inhibits dimerization of the transcriptional activator ToxT. P Natl Acad Sci USA 104: 2372-2377.
283. Shen DK, Saurya S, Wagner C, Nishioka H & Blocker AJ (2010) Domains of the Shigella flexneri type III secretion system IpaB protein involved in secretion regulation. Infect Immun 78: 4999-5010.
284. Skerker JM & Berg HC (2001) Direct observation of extension and retraction of type IV pili. P Natl Acad Sci USA 98: 6901-6904.
285. Sohel I, Puente JL, Ramer SW, Bieber D, Wu CY & Schoolnik GK (1996) Enteropathogenic Escherichia coli: identification of a gene cluster coding for bundle-forming pilus morphogenesis. J Bacteriol 178: 2613-2628.
286. Souza DP, Andrade MO, Alvarez-Martinez CE, Arantes GM, Farah CS & Salinas RK (2011) A component of the Xanthomonadaceae type IV secretion system combines a VirB7 motif with a N0 domain found in outer membrane transport proteins. PLoS Pathog 7: e1002031.
287. Spreter T, Yip CK, Sanowar S et al. (2009) A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat Struct Mol Biol 16: 468-476.
288. Spudich GM, Fernandez D, Zhou XR & Christie PJ (1996) Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. P Natl Acad Sci USA 93: 7512-7517.
289. Stensrud KF, Adam PR, La Mar CD et al. (2008) Deoxycholate interacts with IpaD of Shigella flexneri in inducing the recruitment of IpaB to the type III secretion apparatus needle tip. J Biol Chem 283: 18646-18654.
290. Stimson E, Virji M, Barker S et al. (1996) Discovery of a novel protein modification: alpha-glycerophosphate is a substituent of meningococcal pilin. Biochem J 316: 29-33.
291. Stone KD, Zhang H-Z, Carlson LK & Donnenberg MS (1996) A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus. Mol Microbiol 20: 325-337.
292. Strom MS & Lory S (1991) 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.
293. Strom MS & Lory S (1993) Structure-function and biogenesis of type IV pili. Annu Rev Microbiol 47: 565-596.
294. Strom MS, Nunn DN & 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 90: 2404.
295. Sun H, Zusman DR & Shi W (2000) Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10: 1143-1146.
296. Sung MA, Fleming K, Chen HA & Matthews S (2001) The solution structure of PapGII from uropathogenic Escherichia coli and its recognition of glycolipid receptors. EMBO Rep 2: 621-627.
297. Swietnicki W, Powell BS & Goodin J (2005) Yersinia pestis Yop secretion protein F: purification, characterization, and protective efficacy against bubonic plague. Protein Expr Purif 42: 166-172.
298. Tacket CO, Taylor RK, Losonsky G, Lim Y, Nataro JP, Kaper JB & Levine MM (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.
299. Tato I, Zunzunegui S, de la Cruz F & Cabezon E (2005) TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA dependent ATPase. P Natl Acad Sci USA 102: 8156-8161.
300. Tato I, Matilla I, Arechaga I, Zunzunegui S, de la Cruz F & Cabezon E (2007) The ATPase activity of the DNA transporter TrwB is modulated by protein TrwA: implications for a common assembly mechanism of DNA translocating motors. J Biol Chem 282: 25569-25576.
301. Taylor RK, Miller VL, Furlong DB & Mekalanos JJ (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. P Natl Acad Sci USA 84: 2833-2837.
302. Tchesnokova V, Aprikian P, Kisiela D, Gowey S, Korotkova N, Thomas W & Sokurenko E (2011) Type 1 fimbrial adhesin FimH elicits an immune response that enhances cell adhesion of Escherichia coli. Infect Immun 79: 3895-3904.
303. Tegtmeyer N, Hartig R, Delahay RM et al. (2010) A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation. J Biol Chem 285: 23515-23526.
304. Tegtmeyer N, Wessler S & Backert S (2011) Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J 278: 1190-1202.
305. Terradot L, Bayliss R, Oomen C, Leonard GA, Baron C & Waksman G (2005) Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori. P Natl Acad Sci USA 102: 4956-4961.
306. Thanassi DG, Nuccio S-P, Shu Kin So S & Bäumler AJ (2007) Fimbriae: classification and biochemistry. EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology (Bôck A, Curtiss R III, Kaper JB, Neidhardt FC, Nyström T, Rudd KE & Squires CL, eds). ASM Press, Washington, DC. http://www.ecosal.org.
307. Thomas WE, Trintchina E, Forero M, Vogel V & Sokurenko EV (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109: 913-923.
308. Titball RW & Williamson ED (2001) Vaccination against bubonic and pneumonic plague. Vaccine 19: 4175-4184.
309. Tobiason DM & Seifert HS (2001) Inverse relationship between pilus-mediated gonococcal adherence and surface expression of the pilus receptor, CD46. Microbiology 147: 2333-2340.
310. Tonjum T & Koomey M (1997) The pilus colonization factor of pathogenic neisserial species: organelle biogenesis and structure/function relationships - a review. Gene 192: 155-163.
311. Tonjum T, Freitag NE, Namork E & Koomey M (1995) Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol Microbiol 16: 451-464.
312. Turbyfill KR, Mertz JA, Mallett CP & Oaks EV (1998) Identification of epitope and surface-exposed domains of Shigella flexneri invasion plasmid antigen D (IpaD). Infect Immun 66: 1999-2006.
313. van der Velden AW, Bäumler AJ, Tsolis RM & Heffron F (1998) Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice. Infect Immun 66: 2803-2808.
314. van der Woude M, Braaten B & Low D (1996) Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol 4: 5-9.
315. Varga JJ, Nguyen V, O'Brien DK, Rodgers K, Walker RA & Melville SB (2006) Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other Clostridia. Mol Microbiol 62: 680-694.
316. Veenendaal AK, Hodgkinson JL, Schwarzer L, Stabat D, Zenk SF & Blocker AJ (2007) The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 63: 1719-1730.
317. Verger D, Miller E, Remaut H, Waksman G & Hultgren S (2006) Molecular mechanism of P pilus termination in uropathogenic Escherichia coli. EMBO Rep 7: 1228-1232.
318. Vergunst AC, van Lier MC, den Dulk-Ras A, Grosse Stuve TA, Ouwehand A & Hooykaas PJ (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. P Natl Acad Sci USA 102: 832-837.
319. Vernazza C, Lingard B, Flick-Smith HC, Baillie LW, Hill J & Atkins HS (2009) Small protective fragments of the Yersinia pestis V antigen. Vaccine 27: 2775-2780.
320. Virji M, Makepeace K, Ferguson DJ, Achtman M & Moxon ER (1993) Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol 10: 499-510.
321. Waksman G & Hultgren SJ (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7: 765-774.
322. Wang Y, Zhang L, Picking WL, Picking WD & De Guzman RN (2008) Structural dissection of the extracellular moieties of the type III secretion apparatus. Mol BioSyst 4: 1176-1180.
323. Wang YA, Yu X, Silverman PM, Harris RL & Egelman EH (2009) The structure of F-pili. J Mol Biol 385: 22-29.
324. Warren MJ & Jennings MP (2003) Identification and characterization of pptA: a gene involved in the phase-variable expression of phosphorylcholine on pili of Neisseria meningitidis. Infect Immun 71: 6892-6898.
325. Weeks S, Hill J, Friedlander A & Welkos S (2002) Anti-V antigen antibody protects macrophages from Yersinia pestis-induced cell death and promotes phagocytosis. Microb Pathog 32: 227-237.
326. Weening EH, Cathelyn JS, Kaufman G, Lawrenz MB, Price P, Goldman WE & Miller VL (2011) The dependence of the Yersinia pestis capsule on pathogenesis is influenced by the mouse background. Infect Immun 79: 644-652.
327. Wellens A, Garofalo C, Nguyen H et al. (2008) Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS ONE 3: e2040.
328. Westerlund-Wikstrom B & Korhonen TK (2005) Molecular structure of adhesin domains in Escherichia coli fimbriae. Int J Med Microbiol 295: 479-486.
329. Winans SC & Walker GC (1985) Conjugal transfer system of the IncN plasmid pKM101. J Bacteriol 161: 402-410.
330. Winther-Larsen HC, Wolfgang M, Dunham S et al. (2005) A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol Microbiol 56: 903-917.
331. Wolfgang M, van Putten JP, Hayes SF, Dorward D & Koomey M (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 19: 6408-6418.
332. Worrall LJ, Lameignere E & Strynadka NC (2011) Structural overview of the bacterial injectisome. Curr Opin Microbiol 14: 3-8.
333. Wright KJ, Seed PC & Hultgren SJ (2007) Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9: 2230-2241.
334. Xia Y, Gally D, Forsman-Semb K & Uhlin BE (2000) Regulatory cross-talk between adhesin operons in Escherichia coli: inhibition of type 1 fimbriae expression by the PapB operon. EMBO J 19: 1450-1457.
335. Xu XF, Tan YW, Lam L, Hackett J, Zhang M & Mok YK (2004) NMR structure of a type IVb pilin from Salmonella typhi and its assembly into pilus. J Biol Chem 279: 31599-31605.
336. Yakovenko O, Sharma S, Forero M et al. (2008) FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem 283: 11596-11605.
337. Yen MR, Peabody CR, Partovi SM, Zhai Y, Tseng YH & Saier MH (2002) Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562: 6-31.
338. Yeo HJ, Savvides SN, Herr AB, Lanka E & Waksman G (2000) Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol Cell 6: 1461-1472.
339. Yeo H-J, Yuan Q, Beck MR, Baron C & Waksman G (2003) Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. P Natl Acad Sci USA 100: 15947-15952.
340. Yip CK, Finlay BB & Strynadka NC (2005) Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 12: 75-81.
341. Yoshida T, Furuya N, Ishikura M, Isobe T, Haino-Fukushima K, Ogawa T & Komano T (1998) Purification and characterization of thin pili of IncI1 plasmids ColIb-P9 and R64: formation of PilV-specific cell aggregates by type IV pili. J Bacteriol 180: 2842-2848.
342. Yuan Q, Carle A, Gao C et al. (2005) Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 280: 26349-26359.
343. Zahavi EE, Lieberman JA, Donnenberg MS et al. (2011) Bundle forming pilus retraction enhances enteropathogenic Escherichia coli infectivity. Mol Biol Cell 22: 2436-2447.
344. Zav'yalov V, Zavialov A, Zav'yalova G & Korpela T (2010) Adhesive organelles of Gram-negative pathogens assembled with the classical chaperone/usher machinery: structure and function from a clinical standpoint. FEMS Microbiol Rev 34: 317-378.
345. Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, MacIntyre S & Knight SD (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113: 587-596.
346. Zavialov A, Zav'yalova G, Korpela T & Zav'yalov V (2007) FGL chaperone-assembled fimbrial polyadhesins: anti-immune armament of Gram-negative bacterial pathogens. FEMS Microbiol Rev 31: 478-514.
347. Zhang HZ & Donnenberg MS (1996) DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol Microbiol 21: 787-797.
348. Zhang HZ, Lory S & Donnenberg MS (1994) A plasmid-encoded prepilin peptidase gene from enteropathogenic Escherichia coli. J Bacteriol 176: 6885-6891.
349. Zhang XL, Tsui IS, Yip CM et al. (2000) Salmonella enterica serovar typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun 68: 3067-3073.
350. Zhou G, Mo WJ, Sebbel P et al. (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci 114: 4095-4103.