Structural Characterization of Novel Pseudomonas aeruginosa Type IV Pilins

Journal of Molecular Biology

Volumn 395, Issue 3, 2010, Pages 491-503

  Nguyen, Ylan ^a   Jackson, Sean G ^a   Aidoo, Francisca ^a   Junop, Murray ^a   Burrows, Lori L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

fimbriae; PilA; Pseudomonas aeruginosa; type IV pili; X ray crystallography

Indexed keywords

BACTERIAL PROTEIN; GROUP III PILIN; GROUP V PILIN; PILIN; PROTEIN PILA; TYPE IV PILIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM PILUS; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; MOLECULAR INTERACTION; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; STRUCTURAL HOMOLOGY;

NEISSERIA GONORRHOEAE; PILA; PSEUDOMONAS AERUGINOSA;

EID: 73249123088     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.070     Document Type: Article

References (45)

1. Craig L., Pique M.E., and Tainer J.A. Type IV pilus structure and bacterial pathogenicity. Nat. Rev., Microbiol. 2 (2004) 363-378 doi:10.1038/nrmicro885; nrmicro885 [pii]
2. Pelicic V. Type IV pili: e pluribus unum. Mol. Microbiol. 68 (2008) 827-837 10.1111/j.1365-2958.2008.06197.x
3. Mattick J.S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56 (2002) 289-314 doi:10.1146/annurev.micro.56.012302.160938; 012302.160938 [pii]
4. Craig L., and Li J. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 18 (2008) 267-277 10.1016/j.sbi.2007.12.009
5. Parge H.E., Forest K.T., Hickey M.J., Christensen D.A., Getzoff E.D., and Tainer J.A. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378 (1995) 32-38 10.1038/378032a0
6. Craig L., Volkmann N., Arvai A.S., Pique M.E., Yeager M., Egelman E.H., and Tainer J.A. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 23 (2006) 651-662 S1097-2765(06)00481-3 [pii]; doi:10.1016/j.molcel.2006.07.004
7. Audette G.F., Irvin R.T., and Hazes B. Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture. Biochemistry 43 (2004) 11427-11435 10.1021/bi048957s
8. Keizer D.W., Slupsky C.M., Kalisiak M., Campbell A.P., Crump M.P., Sastry P.A., et al. Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J. Biol. Chem. 276 (2001) 24186-24193 doi:10.1074/jbc.M100659200; M100659200 [pii]
9. Hazes B., Sastry P.A., Hayakawa K., Read R.J., and Irvin R.T. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J. Mol. Biol. 299 (2000) 1005-1017 doi:10.1006/jmbi.2000.3801; S0022-2836(00)93801-4 [pii]
10. Ramboarina S., Fernandes P.J., Daniell S., Islam S., Simpson P., Frankel G., et al. Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J. Biol. Chem. 280 (2005) 40252-40260
11. Craig L., Taylor R.K., Pique M.E., Adair B.D., Arvai A.S., Singh M., et al. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol. Cell 11 (2003) 1139-1150 S1097276503001709 [pii]
12. Xu X.F., Tan Y.W., Lam L., Hackett J., Zhang M., and Mok Y.K. NMR structure of a type IVb pilin from Salmonella typhi and its assembly into pilus. J. Biol. Chem. 279 (2004) 31599-31605 10.1074/jbc.M404727200
13. Harvey H., Habash M., Aidoo F., and Burrows L.L. Single residue changes in the C terminal disulfide-bonded loop of the Pseudomonas aeruginosa type IV pilin influence pilus assembly and twitching motility. J. Bacteriol. 191 (2009) 6513-6524
14. Helaine S., Dyer D.H., Nassif X., Pelicic V., and Forest K.T. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc. Natl Acad. Sci. USA 104 (2007) 15888-15893 10.1073/pnas.0707581104
15. Kohler R., Schafer K., Muller S., Vignon G., Diederichs K., Philippsen A., et al. Structure and assembly of the pseudopilin PulG. Mol. Microbiol. 54 (2004) 647-664 MMI4307 [pii]; doi:10.1111/j.1365-2958.2004.04307.x
16. Yanez M.E., Korotkov K.V., Abendroth J., and Hol W.G. The crystal structure of a binary complex of two pseudopilins: EpsI and EpsJ from the type 2 secretion system of Vibrio vulnificus. J. Mol. Biol. 375 (2008) 471-486 10.1016/j.jmb.2007.10.035
17. Yanez M.E., Korotkov K.V., Abendroth J., and Hol W.G. Structure of the minor pseudopilin EpsH from the type 2 secretion system of Vibrio cholerae. J. Mol. Biol. 377 (2008) 91-103 10.1016/j.jmb.2007.08.041
18. Korotkov K.V., and Hol W.G. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat. Struct. Mol. Biol. 15 (2008) 462-468 10.1038/nsmb.1426
19. Alphonse S., Durand E., Douzi B., Waegele B., Darbon H., Filloux A., et al. Structure of the Pseudomonas aeruginosa XcpT pseudopilin, a major component of the type II secretion system. J. Struct. Biol. (2009) 10.1016/j.jsb.2009.09.003
20. Russell M.A., and Darzins A. The pilE gene product of Pseudomonas aeruginosa, required for pilus biogenesis, shares amino acid sequence identity with the N-termini of type 4 prepilin proteins. Mol. Microbiol. 13 (1994) 973-985
21. Alm R.A., and Mattick J.S. Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol. Microbiol. 16 (1995) 485-496
22. Alm R.A., Hallinan J.P., Watson A.A., and Mattick J.S. Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol. Microbiol. 22 (1996) 161-173
23. Alm R.A., and Mattick J.S. Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa. Gene 192 (1997) 89-98
24. Helaine S., Carbonnelle E., Prouvensier L., Beretti J.L., Nassif X., and 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. 55 (2005) 65-77 10.1111/j.1365-2958.2004.04372.x
25. Pugsley A.P. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57 (1993) 50-108
26. Kus J.V., Tullis E., Cvitkovitch D.G., and Burrows L.L. Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology 150 (2004) 1315-1326
27. Voisin S., Kus J.V., Houliston S., St-Michael F., Watson D., Cvitkovitch D.G., et al. Glycosylation of Pseudomonas aeruginosa strain Pa5196 type IV pilins with mycobacterium-like alpha-1,5-linked d-Araf oligosaccharides. J. Bacteriol. 189 (2007) 151-159 JB.01224-06 [pii]; doi:10.1128/JB.01224-06
28. Castric P. pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology 141 (1995) 1247-1254
29. Kus J.V., Kelly J., Tessier L., Harvey H., Cvitkovitch D.G., and Burrows L.L. Modification of Pseudomonas aeruginosa Pa5196 type IV pilins at multiple sites with d-Araf by a novel GT-C family arabinosyltransferase, TfpW. J. Bacteriol. 190 (2008) 7464-7478 10.1128/JB.01075-08
30. Asikyan M.L., Kus J.V., and Burrows L.L. Novel proteins that modulate type IV pilus retraction dynamics in Pseudomonas aeruginosa. J. Bacteriol. 190 (2008) 7022-7034 10.1128/JB.00938-08
31. Wiehlmann L., Wagner G., Cramer N., Siebert B., Gudowius P., Morales G., et al. Population structure of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 104 (2007) 8101-8106 10.1073/pnas.0609213104
32. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
33. Burrows L.L. A nice return on the "stalk" exchange. Structure 16 (2008) 19-20 10.1016/j.str.2007.12.006
34. Li J., Lim M.S., Li S., Brock M., Pique M.E., Woods Jr. V.L., and Craig L. Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure 16 (2008) 137-148 10.1016/j.str.2007.10.027
35. Giltner C.L., van Schaik E.J., Audette G.F., Kao D., Hodges R.S., Hassett D.J., and Irvin R.T. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol. Microbiol. 59 (2006) 1083-1096 10.1111/j.1365-2958.2005.05002.x
36. Lee K.K., Sheth H.B., Wong W.Y., Sherburne R., Paranchych W., Hodges R.S., et al. The binding of Pseudomonas aeruginosa pili to glycosphingolipids is a tip-associated event involving the C-terminal region of the structural pilin subunit. Mol. Microbiol. 11 (1994) 705-713
37. Audette G.F., van Schaik E.J., Hazes B., and Irvin R.T. DNA-binding protein nanotubes: learning from nature's nanotech examples. Nano Lett. 4 (2004) 1897
38. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138 10.1006/jmbi.1993.1489
39. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in the oscillation mode. Methods Enzymol. 276 (1997) 307
40. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 (2002) 1948-1954
41. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007) 658-674 10.1107/S0021889807021206
42. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132 10.1107/S0907444904019158
43. DeLano W.L. The PyMOL User's Manual (2002), DeLano Scientific, Palo Alto, CA
44. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815 10.1006/jmbi.1993.1626
45. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007) 2947-2948 10.1093/bioinformatics/btm404