Type IV pilin structures: Insights on shared architecture, fiber assembly, receptor binding and type II secretion

Journal of Molecular Microbiology and Biotechnology

Volumn 11, Issue 3-5, 2006, Pages 192-207

  Hansen, Johanna K ^a   Forest, Katrina T ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

3 D protein structure; N. Gonorrhoeae PilE; P. aeruginosa PilA; Type IV pilin

Indexed keywords

PILIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CRYSTAL STRUCTURE; GRAM NEGATIVE BACTERIUM; HYDROPHOBICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLYMERIZATION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SALMONELLA TYPHI; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE;

IVA; NEGIBACTERIA; PILA;

EID: 33748773323     PISSN: 14641801     EISSN: None     Source Type: Journal    
DOI: 10.1159/000094054     Document Type: Review

References (95)

1. Aas FE, Lovold C, Koomey M: 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 2002a;46:1441-1450.
2. Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, Koomey M: Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 2002b;46:749-760.
3. Audette GF, Irvin RT, Hazes B: Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture. Biochemistry 2004;43:11427-11435.
4. Bardy SL, Ng SY, Jarrell KF: Prokaryotic motility structures. Microbiology 2003;149:295-304.
5. Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, Schoolnik G: Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 1998;280:2114-2118.
6. Biswas GD, Sox T, Blackman E, Sparling PF: Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 1977;129:983-992.
7. Blank TE, Zhong H, Bell AL, Whittam TS, Donnenberg MS: Molecular variation among type IV pilin (bfpA) genes from diverse enteropathogenic Escherichia coli strains. Infect Immun 2000;68:7028-7038.
8. Boslego JW, Tramont EC, Chung RC, McChesney DG, Ciak J, Sadoff JC, Piziak MV, Brown JD, Brinton CC Jr, Wood SW, et al: Efficacy trial of a parenteral gonococcal pilus vaccine in man. Vaccine 1991;9:154-162.
9. Bradley DE: A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 1980;26:146-154.
10. Bradley DE, Pitt TL: Pilus-dependence of four Pseudomonas aeruginosa bacteriophages with non-contractile tails. J Gen Virol 1974; 24:1-15.
11. Brinton CC Jr, Bryan J, Dillon J, Guerina N, Jacobson LJ, Labik A, Lee S, Levine A, Lim S, McMichael J, Polen S, Rogers K, To ACC, To SCM: Uses of pili in gonorrhea control: role of bacterial pili in disease, purification and properties of gonococcal pili, and progress in the development of a gonococcal pilus vaccine for gonorrhea; in Brooks GF, Gotschlich EC, Holmes KK, et al (eds): Immunobiology of Neisseria gonorrhoeae. Washington, American Society for Microbiology, 1978, pp 155-178.
12. Buchanan TM, Pierce WA: Pili as a mediator of the attachment of gonococci to human erythrocytes. Infect Immun 1976;13:1483-1489.
13. Campbell AP, Bautista DL, Tripet B, Wong WY, Irvin RT, Hodges RS, Sykes BD: Solution secondary structure of a bacterially expressed peptide from the receptor binding domain of Pseudomonas aeruginosa pili strain PAK: a heteronuclear multidimensional NMR study. Biochemistry 1997a;36:12791-12801.
14. Campbell AP, Wong WY, Houston M Jr, Schweizer F, Cachia PJ, Irvin RT, Hindsgaul O, Hodges RS, Sykes BD: Interaction of the receptor binding domains of Pseudomonas aeruginosa pili strains PAK, PAO, KB7 and P1 to a cross-reactive antibody and receptor analog: implications for synthetic vaccine design. J Mol Biol 1997b;267:382-402.
15. Campbell AP, Wong WY, Irvin RT, Sykes BD: Interaction of a bacterially expressed peptide from the receptor binding domain of Pseudomonas aeruginosa pili strain PAK with a cross-reactive antibody: conformation of the bound peptide. Biochemistry 2000;39:14847-14864.
16. Collins RF, Ford RC, Kitmitto A, Olsen RO, Tonjum T, Derrick JP: Three-dimensional structure of the Neisseria meningitidis secretin PilQ determined from negative-stain transmission electron microscopy. J Bacteriol 2003;185:2611-2617.
17. Collins RF, Frye SA, Balasingham S, Ford RC, Tonjum T, Derrick JP: Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J Biol Chem 2005;280:18923-18930.
18. Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M, Lloyd SJ, Shin DS, Getzoff ED, Yeager M, Forest KT, Tainer JA: Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 2003;11:1139-1150.
19. Craig L, Pique ME, Tainer JA: Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004;2:363-378.
20. Doig P, Todd T, Sastry PA, Lee KK, Hodges RS, Paranchych W, Irvin RT: Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect Immun 1988;56:1641-1646.
21. Doig P, Sastry PA, Hodges RS, Lee KK, Paranchych W, Irvin RT: Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies directed against pili. Infect Immun 1990;58:124-130.
22. Dunlop KV, Irvin RT, Hazes B: Pros and cons of cryocrystallography: should we also collect a room-temperature data set? Acta Crystallogr D Biol Crystallogr 2005;61:80-87.
23. Dupuy B, Taha MK, Possot O, Marchal C, Pugsley AP: PulO, a component of the pullulanase secretion pathway of Klebsiella oxytoca, correctly and efficiently processes gonococcal type IV prepilin in Escherichia coli. Mol Microbiol 1992;6:1887-1894.
24. Filloux A: The underlying mechanisms of type II protein secretion. Biochim Biophys Acta 2004;1694:163-179.
25. Folkhard W, Marvin DA, Watts TH, Paranchych W: Structure of polar pili from Pseudomonas aeruginosa strains K and O. J Mol Biol 1981;149:79-93.
26. Forest KT: Structure and assembly of type IV pilins; in Waksman G, Hultgren SJ, Caparon MG (eds): Structural Basis of Bacterial Pathogenesis. Washington, American Society for Microbiology, 2005, pp 81-100.
27. Forest KT, Tainer JA: Type-4 pilus structure: outside to inside and top to bottom - a mini-review. Gene 1997;192:165-169.
28. Forest KT, Bernstein SL, Getzoff ED, So M, Tribbick G, Geysen HM, Deal CD, Tainer JA: Assembly and antigenicity of the N. gonorrhoeae pilus mapped with antibodies. Infect Immun 1996;64:644-652.
29. Forest KT, Dunham SJ, Koomey M, Tainer JA: Crystallographic structure of phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and morphology. Mol Microbiol 1999;31:743-752.
30. Haas R, Meyer TF: The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 1986;44:107-115.
31. Hazes B, Sastry PA, Hayakawa K, Read RJ, Irwin RT: Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 2000;299:1005-1017.
32. Hegge FT, Hitchen PG, Aas FE, Kristiansen H, Lovold C, Egge-Jacobsen W, Panico M, Leong WY, Bull V, Virji M, Morris HR, Dell A, Koomey M: Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci USA 2004;101:10798-10803.
33. Helaine S, Carbonnelle E, Prouvensier L, Beretti JL, Nassif X, Pelicic V: PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol 2005;55:65-77.
34. Hobbs M, Mattick JS: 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 1993;10:233-243.
35. Howell-Adams B, Seifert HS: Insertion mutations in pilE differentially alter gonococcal pilin antigenic variation. J Bacteriol 1999;181:6133-6141.
36. Jennings MP, Virji M, Evans D, Foster V, Srikhanta YN, Steeghs L, van der Ley P, Moxon ER: Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol Microbiol 1998;29:975-984.
37. Johansson L, Rytkonen A, Bergman P, Albiger B, Kallstrom H, Hokfelt T, Agerberth B, Cattaneo R, Jonsson AB: CD46 in meningococcal disease. Science 2003;301:373-375.
38. Kachlany SC, Planet PJ, Desalle R, Fine DH, Figurski DH, Kaplan JB: flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol 2001;40:542-554.
39. Kaiser D: Bacterial motility: how do pili pull? Curr Biol 2000;10:R777-R780.
40. Kallstrom H, Liszewski MK, Atkinson JP, Jonsson AB: Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria. Mol Microbiol 1997;25:639-647.
41. Keizer DW, Slupsky CM, Kalisiak M, Campbell AP, Crump MP, Sastry PA, Hazes B, Irvin RT, Sykes BD: Structure of a pilin monomer from Pseudomonas aeruginosa - implications for the assembly of pili. J Biol Chem 2001;276:24186-24193.
42. Kim SR, Komano T: The plasmid R64 thin pilus identified as a type IV pilus. J Bacteriol 1997;179:3594-3603.
43. Kirchner M, Meyer TF: The PilC adhesin of the Neisseria type IV pilus-binding specificities and new insights into the nature of the host cell receptor. Mol Microbiol 2005;56:945-957.
44. Kirchner M, Heuer D, Meyer TF: CD46-independent binding of neisserial type IV pili and the major pilus adhesin, PilC, to human epithelial cells. Infect Immun 2005;73:3072-3082.
45. Kirn TJ, Lafferty MJ, Sandoe CMP, Taylor RK: Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 2000;35:896-910.
46. Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T: Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 2003;48:1511-1524.
47. Kohler R, Schafer K, Muller S, Vignon G, Diederichs K, Philippsen A, Ringler P, Pugsley AP, Engel A, Welte W: Structure and assembly of the pseudopilin PulG. Mol Microbiol 2004;54:647-664.
48. Lee KK, Sheth HB, Wong WY, Sherburne R, Paranchych W, Hodges RS, Lingwood CA, Krivan H, Irvin RT: 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 1994;11:705-713.
49. Lyczak JB, Pier GB: Salmonella enterica serovar typhi modulates cell surface expression of its receptor, the cystic fibrosis transmembrane conductance regulator, on the intestinal epithelium. Infect. Immun 2002;70:6416-6423.
50. Maier B, Potter L, So M, Seifert HS, Sheetz MP: Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 2002;99:16012-16017.
51. Maier B, Koomey M, Sheetz MP: A force-dependent switch reverses type IV pilus retraction. Proc Natl Acad Sci USA 2004;101:10961-10966.
52. McInnes C, Sonnichsen FD, Kay CM, Hodges RS, Sykes BD: NMR Solution structure and flexibility of a peptide antigen representing the receptor binding domain of Pseudomonas aeruginosa. Biochemistry 1993;32:13432-13440.
53. Merz AJ, Forest KT: Bacterial surface motility: slime trails, grappling hooks and nozzles. Curr Biol 2002;12:R297-R303.
54. Morand PC, Bille E, Morelle S, Eugene E, Beretti JL, Wolfgang M, Meyer TF, Koomey M, Nassif X: Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J 2004;23:2009-2017.
55. Nassif X, Lowy J, Stenberg P, O'Gaora P, Ganji A, So M: Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol Microbiol 1993;8:719-725.
56. Nouwen N, Ranson N, Saibil H, Wolpensinger B, Engel A, Ghazi A, Pugsley AP: Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proc Natl Acad Sci USA 1999;96:8173-8177.
57. Nudleman E, Kaiser D: Pulling together with type IV pili. J Mol Microbiol Biotechnol 2004;7:52-62.
58. Nunn D, Bergman S, Lory S: Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J Bacteriol 1990;172:2911-2919.
59. O'Toole GA, Kolter R: Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998;30:295-304.
60. Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED, Tainer JA: Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 1995;378:32-38.
61. Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP, Saier MH Jr: Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 2003;149:3051-3072.
62. Pier GB, Grout M, Zaidi T, Meluleni G, Mueschenborn SS, Banting G, Ratcliff R, Evans MJ, Colledge WH: Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 1998;393:79-82.
63. Planet PJ, Kachlany SC, DeSalle R, Figurski DH: Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc Natl Acad Sci USA 2001;98:2503-2508.
64. Possot OM, Vignon G, Bomchil N, Ebel F, Pugsley AP: Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J Bacteriol 2000;182:2142-2152.
65. Power PM, Jennings MP: The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol Lett 2003;218:211-222.
66. Power PM, Roddam LF, Dieckelmann M, Srikhanta YN, Tan YC, Berrington AW, Jennings MP: Genetic characterization of pilin glycosylation in Neisseria meningitidis. Microbiology 2000;146:967-979.
67. Power PM, Roddam LF, Rutter K, Fitzpatrick SZ, Srikhanta YN, Jennings MP: Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis. Mol Microbiol 2003;49:833-847.
68. Pugsley AP: The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 1993a;57:50-108.
69. Pugsley AP: Processing and methylation of PulG, a pilin-like component of the general secretory pathway of Klebsiella oxytoca. Mol Microbiol 1993b;9:295-308.
70. Pugsley AP, Dupuy B: An enzyme with type IV prepilin peptidase activity is required to process components of the general extracellular protein secretion pathway of Klebsiella oxytoca. Mol Microbiol 1992;6:751-760.
71. Rahman M, Kallstrom H, Normark S, Jonsson AB: PilC of pathogenic Neisseria is associated with the bacterial cell surface. Mol Microbiol 1997;25:11-25.
72. Ramboarina S, Fernandes PJ, Daniell S, Islam S, Simpson P, Frankel G, Booy F, Donnenberg MS, Matthews S: Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem 2005;280:40252-40260.
73. Rhine JA, Taylor RK: TcpA pilin sequences and colonization requirements for O1 and O139 Vibrio cholerae. Mol Microbiol 1994;13:1013-1020.
74. Rini JM: Lectin structure. Annu Rev Biophys Biomol Struct 1995;24:551-577.
75. Rudel T, Scheuerpflug I, Meyer TF: Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 1995;373:357-359.
76. Sandkvist M: Biology of type II secretion. Mol Microbiol 2001;40:271-283.
77. Sauvonnet N, Vignon G, Pugsley AP, Gounon P: Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 2000;19:2221-2228.
78. 1 on epithelial cells. Infect Immun 2001;69:719-729.
79. Segal E, Hagblom P, Seifert HS, So M: Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc Natl Acad Sci USA 1986;83:2177-2181.
80. Stimson E, Virji M, Makepeace K, Dell A, Morris HR, Payne G, Saunders JR, Jennings MP, Barker S, Panico M, Blench I, Moxon ER: Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol 1995;17:1201-1214.
81. Strom MS, Bergman P, Lory S: Identification of active-site cysteines in the conserved domain of PilD, the bifunctional type IV pilin leader peptidase/N-methyltransferase of Pseudomonas aeruginosa. J Biol Chem 1993a;268:15788-15794.
82. Strom MS, Nunn DN, Lory S: A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 1993b;90:2404-2408.
83. Suh JY, Spyracopoulos L, Keizer DW, Irvin RT, Sykes BD: Backbone dynamics of receptor binding and antigenic regions of a Pseudomonas aeruginosa pilin monomer. Biochemistry 2001;40:3985-3995.
84. Swanson J: Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med 1973;137:571-589.
85. Swanson J, Robbins K, Barrera O, Koomey JM: Gene conversion variations generate structurally distinct pilin polypeptides in Neisseria gonorrhoeae. J Exp Med 1987;165:1016-1025.
86. Taylor RK, Kirn TJ, Meeks MD, Wade TK, Wade WF: A Vibrio cholerae classical TcpA amino acid sequence induces protective antibody that binds an area hypothesized to be important for toxin-coregulated pilus structure. Infect Immun 2004;72:6050-6060.
87. Tennent JM, Mattick JS: Type 4 fimbriae; in Klemm P (ed): Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. Boca Raton, CRC Press, 1994, pp 127-146.
88. Tsui IS, Yip CM, Hackett J, Morris C: The type IVB pili of Salmonella enterica serovar typhi bind to the cystic fibrosis transmembrane conductance regulator. Infect Immun 2003;71:6049-6050.
89. Van Schaik EJ, Giltner CL, Audette GF, Keizer DW, Bautista DL, Slupsky CM, Sykes BD, Irvin RT: DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 2005;187:1455-1464.
90. Vignon G, Kohler R, Larquet E, Giroux S, Prevost MC, Roux P, Pugsley AP: Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides. J Bacteriol 2003;185:3416-3428.
91. Weiser JN, Goldberg JB, Pan N, Wilson L, Virji M: The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect Immun 1998;66:4263-4267.
92. Winther-Larsen HC, Hegge FT, Wolfgang M, Hayes SF, van Putten JP, Koomey M: Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 1998;98:15276-15281.
93. Winther-Larsen HC, Wolfgang M, Dunham S, van Putten JP, Dorward D, Lovold C, Aas FE, Koomey M: A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol Microbiol 2005;56:903-917.
94. Xu XF, Tan YW, Lam L, Hackett J, Zhang M, Mok YK: NMR structure of a type IVb pilin from Salmonella typhi and its assembly into pilus. J Biol Chem 2004;279:31599-31605.
95. Zhang XL, Tsui IS, Yip CM, Fung AW, Wong DK, Dai X, Yang Y, Hackett J, Morris C: Salmonella enterica serovar typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun 2000;68:3067-3073.