Substitutions in the N-terminal alpha helical spine of Neisseria gonorrhoeae pilin affect Type IV pilus assembly, dynamics and associated functions

Molecular Microbiology

Volumn 63, Issue 1, 2007, Pages 69-85

  Aas, Finn Erik ^a   Winther Larsen, Hanne C ^a   Wolfgang, Matthew ^b   Frye, Stephan ^a   Løvold, Cecilia ^a   Roos, Norbert ^a   Van Putten, Jos P M ^c   Koomey, Michael ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PILIN; POLYMER;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL ORGANELLE; DYNAMICS; GENETIC TRANSFORMATION; GENETICS; MEMBRANE; MOLECULAR INTERACTION; NEISSERIA GONORRHOEAE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SUBSTITUTION REACTION; WILD TYPE;

AMINO ACID SUBSTITUTION; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; NEISSERIA GONORRHOEAE;

NEGIBACTERIA; NEISSERIA GONORRHOEAE;

EID: 33845688257     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05482.x     Document Type: Article

References (56)

1. Aas, F.E., Løvold, C., and Koomey, M. (2002a) 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. Aas, F.E., Wolfgang, M., Frye, S., Dunham, S., Løvold, C., and Koomey, M. (2002b) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46: 749-760.
3. Bradley, D.E. (1972a) Stimulation of pilus formation in Pseudomonas aeruginosa by RNA bacteriophage adsorption. Biochem Biophys Res Commun 47: 1080-1087.
4. Bradley, D.E. (1972b) Evidence for the retraction of Pseudomonas aeruginosa RNA phage pili. Biochem Biophys Res Commun 47: 142-149.
5. Bradley, D.E. (1972c) Shortening of Pseudomonas aeruginosa pili after RNA-phage adsorption. J Gen Microbiol 72: 303-319.
6. Chen, I., and Dubnau, D. (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2: 241-249.
7. Chen, I., Provvedi, R., and Dubnau, D. (2006) A macromolecular complex formed by pilin-like protein in competent Bacillus subtilis. J Biol Chem 281: 21720-21727.
8. Chiang, S.L., Taylor, R.K., Koomey, M., and Mekalanos, J.J. (1995) Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Mol Microbiol 17: 1133-1142.
9. Close, T.J., and Rodriguez, R.L. (1982) Construction and characterization of the chloramphenicol-resistance gene cartridge: a new approach to the transcriptional mapping of extrachromosomal elements. Gene 20: 305-316.
10. Craig, L., Taylor, R.K., Pique, M.E., Adair, B.D., Arvai, A.S., Singh, M., 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.
11. Craig, L., Pique, M.E., and Tainer, J.A. (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2: 363-378.
12. Drake, S.L., and Koomey, M. (1995) The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol Microbiol 18: 975-986.
13. Drake, S.L., Sandstedt, S.A., and Koomey, M. (1997) PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae, affects expression of PilQ as a high-molecular-mass multimer. Mol Microbiol 23: 657-668.
14. Durand, E., Bernadac, A., Ball, G., Lazdunski, A., Sturgis, J.N., and Filloux, A. (2003) Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J Bacteriol 185: 2749-2758.
15. Freitag, N.E., Seifert, H.S., and Koomey, M. (1995) Characterization of the pilF-pilD pilus-assembly locus of Neisseria gonorrhoeae. Mol Microbiol 16: 575-586.
16. Haas, R., Schwarz, H., and Meyer, T.F. (1987) Release of soluble pilin antigen coupled with gene conversion in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 84: 9079-9083.
17. Hazes, B., Sastry, P.A., Hayakawa, K., Read, R.J., and Irvin, R.T. (2000) Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 299: 1005-1017.
18. Hegge, F.T., Hitchen, P.G., Aas, F.E., Kristiansen, H., Løvold, C., Egge-Jacobsen, W., et al. (2004) Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci USA 101: 10798-10803.
19. Horiuchi, T., and Komano, T. (1998) Mutational analysis of plasmid R64 thin pilus prepilin: the entire prepilin sequence is required for processing by type IV prepilin peptidase. J Bacteriol 180: 4613-4620.
20. Jones, C.H., Danese, P.N., Pinkner, J.S., Silhavy, T.J., and Hultgren, S.J. (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16: 6394-6406.
21. Keizer, D.W., Slupsky, C.M., Kalisiak, M., Campbell, A.P., Crump, M.P., Sastry, P.A., et al. (2001) Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J Biol Chem 276: 24186-24193.
22. Kirn, T.J., Lafferty, M.J., Sandoe, C.M., and Taylor, R.K. (2000) Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 35: 896-910.
23. Kohler, R., Schafer, K., Muller, S., Vignon, G., Diederichs, K., Philippsen, A., et al. (2004) Structure and assembly of the pseudopilin PulG. Mol Microbiol 54: 647-664.
24. Koomey, M., and Falkow, S. (1987) Cloning of the recA gene of Neisseria gonorrhoeae and construction of gonococcal recA mutants. J Bacteriol 169: 790-795.
25. Koomey, M., Bergstrom, S., Blake, M., and Swanson, J. (1991) Pilin expression and processing in pilus mutants of Neisseria gonorrhoeae: critical role of Gly-1 in assembly. Mol Microbiol 5: 279-287.
26. Lauer, P., Albertson, N.H., and Koomey, M. (1993) Conservation of genes encoding components of a type IV pilus assembly/two-step protein export pathway in Neisseria gonorrhoeae. Mol Microbiol 8: 357-368.
27. Long, C.D., Tobiason, D.M., Lazio, M.P., Kline, K.A., and Seifert, H.S. (2003) Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infect Immun 71: 6279-6291.
28. Macdonald, D.L., Pasloske, B.L., and 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.
29. Mattick, J.S. (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56: 289-314.
30. Merz, A.J., and Forest, K.T. (2002) Bacterial surface motility: slime trails, grappling hooks and nozzles. Curr Biol 12: R297-R303.
31. Merz, A.J., So, M., and Sheetz, M.P. (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102.
32. Parge, H.E., Forest, K.T., Hickey, M.J., Christensen, D.A., Getzoff, E.D., and Tainer, J.A. (1995) Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378: 32-38.
33. Park, H.S., Wolfgang, M., van Putten, J.P., Dorward, D., Hayes, S.F., and Koomey, M. (2001) Structural alterations in a type IV pilus subunit protein result in concurrent defects in multicellular behaviour and adherence to host tissue. Mol Microbiol 42: 293-307.
34. Park, H.S., Wolfgang, M., and Koomey, M. (2002) Modification of type IV pilus-associated epithelial cell adherence and multicellular behavior by the PilU protein of Neisseria gonorrhoeae. Infect Immun 70: 3891-3903.
35. Pasloske, B.L., and Paranchych, W. (1988) The expression of mutant pilins in Pseudomonas aeruginosa: fifth position glutamate affects pilin methylation. Mol Microbiol 2: 489-495.
36. Pasloske, B.L., Scraba, D.G., and Paranchych, W. (1989) Assembly of mutant pilins in Pseudomonas aeruginosa: formation of pili composed of heterologous subunits. J Bacteriol 171: 2142-2147.
37. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
38. van Putten, J.P., and Paul, S.M. (1995) Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J 14: 2144-2154.
39. Ramboarina, S., Fernandes, P.J., Daniell, S., Islam, S., Simpson, P., Frankel, G., et al. (2005) Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem 280: 40252-40260.
40. Rudel, T., Facius, D., Barten, R., Scheuerpflug, I., Nonnenmacher, E., and Meyer, T.F. (1995) Role of pili and the phase-variable PilC protein in natural competence for transformation of Neisseria gonorrhoeae. Proc Natl Acad Sci USA 92: 7986-7990.
41. Sandkvist, M. (2001) Biology of type II secretion. Mol Microbiol 40: 271-283.
42. Sauvonnet, N., Vignon, G., Pugsley, A.P., and Gounon, P. (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 19: 2221-2228.
43. Seifert, H.S., Ajioka, R.S., Paruchuri, D., Heffron, F., and So, M. (1990) Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J Bacteriol 172: 40-46.
44. Skerker, J.M., and Berg, H.C. (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 98: 6901-6904.
45. Stein, D.C., Danaher, R.J., and Cook, T.M. (1991) Characterization of a gyrB mutation responsible for low-level nalidixic acid resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 35: 622-626.
46. Strom, M.S., and 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.
47. Strom, M.S., Nunn, D.N., and 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 USA 90: 2404-2408.
48. Tonjum, T., Freitag, N.E., Namork, E., and Koomey, M. (1995) Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol Microbiol 16: 451-464.
49. Vignon, G., Kohler, R., Larquet, E., Giroux, S., Prevost, M.C., Roux, P., and Pugsley, A.P. (2003) 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.
50. Winther-Larsen, H.C., Hegge, F.T., Wolfgang, M., Hayes, S.F., van Putten, J.P., and Koomey, M. (2001) Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 98: 15276-15281.
51. Winther-Larsen, H.C., Wolfgang, M., Dunham, S., van Putten, J.P., Dorward, D., Løvold, C., 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.
52. Wolfgang, M., Park, H.S., Hayes, S.F., van Putten, J.P., and Koomey, M. (1998a) Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 95: 14973-14978.
53. Wolfgang, M., Lauer, P., Park, H.S., Brossay, L., Hebert, J., and Koomey, M. (1998b) PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29: 321-330.
54. Wolfgang, M., van Putten, J.P., Hayes, S.F., and Koomey, M. (1999) The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol Microbiol 31: 1345-1357.
55. Wolfgang, M., van Putten, J.P., Hayes, S.F., Dorward, D., and Koomey, M. (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 19: 6408-6418.
56. Zhang, Q.Y., DeRyckere, D., Lauer, P., and Koomey, M. (1992) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Natl Acad Sci USA 89: 5366-5370.