Structure/function analysis of Neisseria meningitidis PilW, a conserved protein that plays multiple roles in type IV pilus biology

Infection and Immunity

Volumn 79, Issue 8, 2011, Pages 3028-3035

  Szeto, Tim H ^a   Dessen, Andréa ^b   Pelicic, Vladimir ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PILW PROTEIN; SECRETIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM PILUS; BIOGENESIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; MEMBRANE STABILIZATION; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE;

DNA MUTATIONAL ANALYSIS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NEISSERIA MENINGITIDIS;

EID: 79961101471     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05313-11     Document Type: Article

References (47)

1. Arts, J., R. van Boxtel, A. Filloux, J. Tommassen, and M. Koster. 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.
2. Brown, D., S. Helaine, E. Carbonnelle, and V. Pelicic. 2010. Systematic functional analysis reveals that a set of 7 genes is involved in fine tuning of the multiple functions mediated by type IV pili in Neisseria meningitidis. Infect. Immun. 78, 3053-3063.
3. Burrows, L. L. 2005. Weapons of mass retraction. Mol. Microbiol. 57, 878-888.
4. Carbonnelle, E., S. Helaine, X. Nassif, and V. Pelicic. 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.
5. Carbonnelle, E., S. Helaine, L. Prouvensier, X. Nassif, and V. Pelicic. 2005. Type IV pilus biogenesis in Neisseria meningitidis, PilW is involved in a step occurring after pilus assembly, essential for fiber stability and function. Mol. Microbiol. 55, 54-64.
6. Cegelski, L., et al. 2009. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 5, 913-919.
7. Collin, S., I. Guilvout, N. N. Nickerson, and A. P. Pugsley. 2011. Sorting of an integral outer membrane protein via the lipoprotein-specific Lol pathway and a dedicated lipoprotein pilotin. Mol. Microbiol. 80, 655-665.
8. Collins, R. F., et al. 2005. Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J. Biol. Chem. 280, 18923-18930.
9. Craig, L., and J. Li. 2008. Type IV pili, paradoxes in form and function. Curr. Opin. Struct. Biol. 18, 267-277.
10. Craig, L., M. E. Pique, and J. A. Tainer. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2, 363-378.
11. Daefler, S., I. Guilvout, K. R. Hardie, A. P. Pugsley, and M. Russel. 1997. The C-terminal domain of the secretin PulD contains the binding site for its cognate chaperone, PulS, and confers PulS dependence on pIVf1 function. Mol. Microbiol. 24, 465-475.
12. D'Andrea, L. D., and L. Regan. 2003. TPR proteins, the versatile helix. Trends Biochem. Sci. 28, 655-662.
13. Francetic, O., N. Buddelmeijer, S. Lewenza, C. A. Kumamoto, and A. P. Pugsley. 2007. Signal recognition particle-dependent inner membrane targeting of the PulG pseudopilin component of a type II secretion system. J. Bacteriol. 189, 1783-1793.
14. Frye, S. A., et al. 2006. Topology of the outer-membrane secretin PilQ from Neisseria meningitidis. Microbiology 152, 3751-3764.
15. Geoffroy, M., S. Floquet, A. Métais, X. Nassif, and V. Pelicic. 2003. Largescale analysis of the meningococcus genome by gene disruption, resistance to complement-mediated lysis. Genome Res. 13, 391-398.
16. Guilvout, I., M. Chami, A. Engel, A. P. Pugsley, and N. Bayan. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25, 5241-5249.
17. Hardie, K. R., S. Lory, and A. P. Pugsley. 1996. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15, 978-988.
18. Hardie, K. R., A. Seydel, I. Guilvout, and A. P. Pugsley. 1996. The secretin-specific, chaperone-like protein of the general secretory pathway, separation of proteolytic protection and piloting functions. Mol. Microbiol. 22, 967-976.
19. Helaine, S., D. H. Dyer, X. Nassif, V. Pelicic, and K. T. Forest. 2007. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc. Natl. Acad. Sci. U. S. A. 104, 15888-15893.
20. Juncker, A. S., et al. 2003. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12, 1652-1662.
21. Kim, K., et al. 2006. Crystal structure of PilF, functional implication in the type 4 pilus biogenesis in Pseudomonas aeruginosa. Biochem. Biophys. Res. Commun. 340, 1028-1038.
22. Koo, J., et al. 2008. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin. J. Bacteriol. 190, 6961-6969.
23. Lario, P. I., et al. 2005. Structure and biochemical analysis of a secretin pilot protein. EMBO J. 24, 1111-1121.
24. Long, C. D., et al. 2001. Modulation of gonococcal piliation by regulatable transcription of pilE. J. Bacteriol. 183, 1600-1609.
25. Maier, B., et al. 2002. Single pilus motor forces exceed 100 pN. Proc. Natl. Acad. Sci. U. S. A. 99, 16012-16017.
26. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289-314.
27. Mehr, I. J., C. D. Long, C. D. Serkin, and H. S. Seifert. 2000. A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics 154, 523-532.
28. Merz, A. J., M. So, and M. P. Sheetz. 2000. Pilus retraction powers bacterial twitching motility. Nature 407, 98-102.
29. Morand, P. C., P. Tattevin, E. Euge'ne, J.-L. Beretti, and X. Nassif. 2001. The adhesive property of the type IV pilus-associated component PilC1 of pathogenic Neisseria is supported by the conformational structure of the N-terminal part of the molecule. Mol. Microbiol. 40, 846-856.
30. Nassif, X., et al. 1994. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 91, 3769-3773.
31. Nassif, X., et al. 1993. Antigenic variation of pilin regulates adhesion of Neisseria meningitidis to human epithelial cells. Mol. Microbiol. 8, 719-725.
32. Nudleman, E., D. Wall, and D. Kaiser. 2006. Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol. Microbiol. 60, 16-29.
33. Pelicic, V. 2008. Type IV pili, e pluribus unum? Mol. Microbiol. 68, 827-837.
34. Pinkner, J. S., et al. 2006. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc. Natl. Acad. Sci. U. S. A. 103, 17897-17902.
35. Pujol, C., E. Euge'ne, L. de Saint Martin, and X. Nassif. 1997. Interaction of Neisseria meningitidis with a polarized monolayer of epithelial cells. Infect. Immun. 65, 4836-4842.
36. Rodriguez-Soto, J. P., and D. Kaiser. 1997. Identification and localization of the Tgl protein, which is required for Myxococcus xanthus social motility. J. Bacteriol. 179, 4372-4381.
37. Rusniok, C., et al. 2009. NeMeSys, a resource for narrowing the gap between sequence and function in the human pathogen Neisseria meningitidis. Genome Biol. 10, R110.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning, a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Satyshur, K. A., et al. 2007. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 15, 363-376.
40. Soto, G. E., and S. J. Hultgren. 1999. Bacterial adhesins, common themes and variations in architecture and assembly. J. Bacteriol. 181, 1059-1071.
41. Strom, M. S., D. N. Nunn, and S. Lory. 1993. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl. Acad. Sci. U. S. A. 90, 2404-2408.
42. Trindade, M. B., V. Job, C. Contreras-Martel, V. Pelicic, and A. Dessen. 2008. Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers. J. Mol. Biol. 378, 1031-1039.
43. Turner, L. R., J. C. Lara, D. N. Nunn, and S. Lory. 1993. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 175, 4962-4969.
44. Winther-Larsen, H. C., et al. 2001. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl. Acad. Sci. U. S. A. 98, 15276-15281.
45. Wolfgang, M., et al. 1998. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol. Microbiol. 29, 321-330.
46. Wolfgang, M., H. S. Park, S. F. Hayes, J. P. van Putten, and M. Koomey. 1998. 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. U. S. A. 95, 14973-14978.
47. Wolfgang, M., J. P. van Putten, S. F. Hayes, D. Dorward, and M. Koomey. 2000. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 19, 6408-6418.