PilM/N/O/P Proteins Form an Inner Membrane Complex That Affects the Stability of the Pseudomonas aeruginosa Type IV Pilus Secretin

Journal of Molecular Biology

Volumn 394, Issue 1, 2009, Pages 128-142

  Ayers, M ^a,b   Sampaleanu, L M ^c   Tammam, S ^c,d   Koo, J ^c,d   Harvey, H ^a,b   Howell, P L ^c,d   Burrows, L L ^a,b,c  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

PilM PilN PilO PilP; pilus biogenesis; Pseudomonas aeruginosa; type II secretion; type IV pili

Indexed keywords

BACTERIAL PROTEIN; PILIN; PILM PROTEIN; PILN PROTEIN; PILO PROTEIN; PILP PROTEIN; SECRETIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM PILUS; COMPLEX FORMATION; CONTROLLED STUDY; MEMBRANE STABILIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; STOICHIOMETRY; TYPE IV SECRETION SYSTEM; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); IVA; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; CELL MEMBRANE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; MODELS, MOLECULAR; MOVEMENT; MUTATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA;

EID: 70350141013     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.09.034     Document Type: Article

References (83)

1. Pelicic V. Type IV pili: e pluribus unum?. Mol. Microbiol. 68 (2008) 827-837 10.1111/j.1365-2958.2008.06197.x
2. O'Toole G.A., and Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30 (1998) 295-304
3. Han X., Kennan R.M., Parker D., Davies J.K., and Rood J.I. Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus. J. Bacteriol. 189 (2007) 5022-5033 10.1128/JB.00138-07
4. Hager A.J., Bolton D.L., Pelletier M.R., Brittnacher M.J., Gallagher L.A., Kaul R., et al. Type IV pili-mediated secretion modulates Francisella virulence. Mol. Microbiol. 62 (2006) 227-237 10.1111/j.1365-2958.2006.05365.x
5. Strom M.S., and Lory S. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47 (1993) 565-596 10.1146/annurev.mi.47.100193.003025 [doi]
6. Long C.D., Tobiason D.M., Lazio M.P., Kline K.A., and Seifert H.S. Low-level pilin expression allows for substantial DNA transformation competence in Neisseria gonorrhoeae. Infect. Immun. 71 (2003) 6279-6291
7. Friedrich A., Prust C., Hartsch T., Henne A., and Averhoff B. Molecular analyses of the natural transformation machinery and identification of pilus structures in the extremely thermophilic bacterium Thermus thermophilus strain HB27. Appl. Environ. Microbiol. 68 (2002) 745-755
8. Hobbs M., and Mattick J.S. 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 (1993) 233-243
9. Costerton J.W., Stewart P.S., and Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 284 (1999) 1318-1322
10. Chiang P., and Burrows L.L. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J. Bacteriol. 185 (2003) 2374-2378
11. Merz A.J., So M., and Sheetz M.P. Pilus retraction powers bacterial twitching motility. Nature 407 (2000) 98-102
12. Semmler A.B., Whitchurch C.B., and Mattick J.S. A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145 (1999) 2863-2873
13. Mattick J.S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56 (2002) 289-314
14. Harshey R.M. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57 (2003) 249-273 10.1146/annurev.micro.57.030502.091014
15. Craig L., Pique M.E., and Tainer J.A. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2 (2004) 363-378 10.1038/nrmicro885 [doi]; nrmicro885 [pii]
16. Manning P.A. The tcp gene cluster of Vibrio cholerae. Gene 192 (1997) 63-70
17. Zhang X.L., Tsui I.S., Yip C.M., Fung A.W., Wong D.K., Dai X., et al. Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. Infect. Immun. 68 (2000) 3067-3073
18. Bieber D., Ramer S.W., Wu C.Y., Murray W.J., Tobe T., Fernandez R., and Schoolnik G.K. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280 (1998) 2114-2118
19. Burrows L.L. Weapons of mass retraction. Mol. Microbiol. 57 (2005) 878-888 MMI4703 [pii]; 10.1111/j.1365-2958.2005.04703.x [doi]
20. Nudleman E., Wall D., and Kaiser D. Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol. Microbiol. 60 (2006) 16-29 MMI5095 [pii]; 10.1111/j.1365-2958.2006.05095.x [doi]
21. Carbonnelle E., Helaine S., Nassif X., and Pelicic V. 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 (2006) 1510-1522 MMI5341 [pii]; 10.1111/j.1365-2958.2006.05341.x [doi]
22. Bakaletz L.O., Baker B.D., Jurcisek J.A., Harrison A., Novotny L.A., Bookwalter J.E., et al. Demonstration of type IV pilus expression and a twitching phenotype by Haemophilus influenzae. Infect. Immun. 73 (2005) 1635-1643 10.1128/IAI.73.3.1635-1643.2005
23. Boyd J.M., Dacanay A., Knickle L.C., Touhami A., Brown L.L., Jericho M.H., et al. Contribution of type IV pili to the virulence of Aeromonas salmonicida subsp. salmonicida in Atlantic salmon (Salmo salar L.). Infect. Immun. 76 (2008) 1445-1455 10.1128/IAI.01019-07
24. Rumszauer J., Schwarzenlander C., and Averhoff B. Identification, subcellular localization and functional interactions of PilMNOWQ and PilA4 involved in transformation competency and pilus biogenesis in the thermophilic bacterium Thermus thermophilus HB27. FEBS J. 273 (2006) 3261-3272 10.1111/j.1742-4658.2006.05335.x
25. Martin P.R., Hobbs M., Free P.D., Jeske Y., and Mattick J.S. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 9 (1993) 857-868
26. Martin P.R., Watson A.A., McCaul T.F., and Mattick J.S. Characterization of a five-gene cluster required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 16 (1995) 497-508
27. Lewenza S., Mhlanga M.M., and Pugsley A.P. Novel inner membrane retention signals in Pseudomonas aeruginosa lipoproteins. J. Bacteriol. 190 (2008) 6119-6125 10.1128/JB.00603-08
28. Peabody C.R., Chung Y.J., Yen M.R., Vidal-Ingigliardi D., Pugsley A.P., and Saier Jr. M.H. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149 (2003) 3051-3072
29. Russel M. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 279 (1998) 485-499
30. Turner L.R., Lara J.C., Nunn D.N., and Lory S. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 175 (1993) 4962-4969
31. Whitchurch C.B., Hobbs M., Livingston S.P., Krishnapillai V., and Mattick J.S. Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. Gene 101 (1991) 33-44 0378-1119(91)90221-V [pii]
32. Whitchurch C.B., and Mattick J.S. Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa. Mol. Microbiol. 13 (1994) 1079-1091
33. 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
34. 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
35. Alm R.A., and Mattick J.S. Identification of two genes with prepilin-like leader sequences involved in type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 178 (1996) 3809-3817
36. 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
37. Winther-Larsen H.C., Wolfgang M., Dunham S., van Putten J.P., Dorward D., Lovold C., et al. A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol. Microbiol. 56 (2005) 903--917 . 10.1111/j.1365-2958.2005.04591.x
38. Py B., Loiseau L., and Barras F. An inner membrane platform in the type II secretion machinery of Gram-negative bacteria. EMBO Rep. 2 (2001) 244-248 10.1093/embo-reports/kve042
39. Johnson T.L., Abendroth J., Hol W.G., and Sandkvist M. Type II secretion: from structure to function. FEMS Microbiol. Lett. 255 (2006) 175-186 10.1111/j.1574-6968.2006.00102.x
40. Filloux A. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694 (2004) 163-179 10.1016/j.bbamcr.2004.05.003
41. Crowther L.J., Anantha R.P., and Donnenberg M.S. The inner membrane subassembly of the enteropathogenic Escherichia coli bundle-forming pilus machine. Mol. Microbiol. 52 (2004) 67-79
42. Douet V., Loiseau L., Barras F., and Py B. Systematic analysis, by the yeast two-hybrid, of protein interaction between components of the type II secretory machinery of Erwinia chrysanthemi. Res. Microbiol. 155 (2004) 71-75 10.1016/j.resmic.2003.10.001
43. Possot O.M., Vignon G., Bomchil N., Ebel F., and Pugsley A.P. Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J. Bacteriol. 182 (2000) 2142-2152
44. Sandkvist M., Keith J.M., Bagdasarian M., and Howard S.P. Two regions of EpsL involved in species-specific protein-protein interactions with EpsE and EpsM of the general secretion pathway in Vibrio cholerae. J. Bacteriol. 182 (2000) 742-748
45. Robert V., Filloux A., and Michel G.P. Subcomplexes from the Xcp secretion system of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 252 (2005) 43-50 S0378-1097(05)00580-X [pii]; 10.1016/j.femsle.2005.08.029 [doi]
46. Abendroth J., Bagdasarian M., Sandkvist M., and Hol W.G. The structure of the cytoplasmic domain of EpsL, an inner membrane component of the type II secretion system of Vibrio cholerae: an unusual member of the actin-like ATPase superfamily. J. Mol. Biol. 344 (2004) 619-633 S0022-2836(04)01220-3 [pii]; 10.1016/j.jmb.2004.09.062 [doi]
47. Sampaleanu L.M., Bonanno J.B., Ayers M., Koo J., Tammam S., Burley S.K., et al. Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex. J. Mol. Biol. 394 (2009) 143-159
48. Perrakis A., Morris R., and Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6 (1999) 458-463 10.1038/8263
49. Woodruff W.A., and Hancock R.E. Construction and characterization of Pseudomonas aeruginosa protein F-deficient mutants after in vitro and in vivo insertion mutagenesis of the cloned gene. J. Bacteriol. 170 (1988) 2592-2598
50. Clancy M.J., and Newton A. Localization of proteins in the inner and outer membranes of Caulobacter crescentus. Biochim. Biophys. Acta 686 (1982) 160-169
51. Lybarger S.R., Johnson T.L., Gray M.D., Sikora A.E., and Sandkvist M. Docking and assembly of the type II secretion complex of Vibrio cholerae. J. Bacteriol. 191 (2009) 3149-3161 10.1128/JB.01701-08
52. Kutter S., Buhrdorf R., Haas J., Schneider-Brachert W., Haas R., and Fischer W. Protein subassemblies of the Helicobacter pylori Cag type IV secretion system revealed by localization and interaction studies. J. Bacteriol. 190 (2008) 2161-2171 10.1128/JB.01341-07
53. Tonjum T., Caugant D.A., Dunham S.A., and Koomey M. Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol. Microbiol. 29 (1998) 111-124
54. Hancock R.E., and Nikaido H. Outer membranes of Gram-negative bacteria: XIX. Isolation from Pseudomonas aeruginosa PAO1 and use in reconstitution and definition of the permeability barrier. J. Bacteriol. 136 (1978) 381-390
55. Kehl-Fie T.E., Porsch E.A., Miller S.E., and St Geme III J.W. Expression of Kingella kingae type IV pili is regulated by {sigma}54, PilS, and PilR. J. Bacteriol. (2009) 10.1128/JB.00123-09
56. Ishimoto K.S., and Lory S. Identification of pilR, which encodes a transcriptional activator of the Pseudomonas aeruginosa pilin gene. J. Bacteriol. 174 (1992) 3514-3521
57. Boyd J.M., and Lory S. Dual function of PilS during transcriptional activation of the Pseudomonas aeruginosa pilin subunit gene. J. Bacteriol. 178 (1996) 831-839
58. Koga T., Ishimoto K., and Lory S. Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili. Infect. Immun. 61 (1993) 1371-1377
59. Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37 (2009) D412
60. Castric P.A., and Deal C.D. Differentiation of Pseudomonas aeruginosa pili based on sequence and B-cell epitope analyses. Infect. Immun. 62 (1994) 371-376
61. 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
62. 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
63. 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
64. Lara B., Rico A.I., Petruzzelli S., Santona A., Dumas J., Biton J., et al. Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol. Microbiol. 55 (2005) 699-711
65. Michel G., Bleves S., Ball G., Lazdunski A., and Filloux A. Mutual stabilization of the XcpZ and XcpY components of the secretory apparatus in Pseudomonas aeruginosa. Microbiology 144 (1998) 3379-3386
66. Abendroth J., Bagdasarian M., Sandkvist M., and Hol W.G. The structure of the cytoplasmic domain of EpsL, an inner membrane component of the type II secretion system of Vibrio cholerae: an unusual member of the actin-like ATPase superfamily. J. Mol. Biol. 344 (2004) 619-633 S0022-2836(04)01220-3 [pii]; 10.1016/j.jmb.2004.09.062 [doi]
67. Abendroth J., Murphy P., Sandkvist M., Bagdasarian M., and Hol W.G. The X-ray structure of the type II secretion system complex formed by the N-terminal domain of EpsE and the cytoplasmic domain of EpsL of Vibrio cholerae. J. Mol. Biol. 348 (2005) 845-855 S0022-2836(05)00243-3 [pii]; 10.1016/j.jmb.2005.02.061 [doi]
68. Balasingham S.V., Collins R.F., Assalkhou R., Homberset H., Frye S.A., Derrick J.P., and Tonjum T. Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J. Bacteriol. 189 (2007) 5716-5727 10.1128/JB.00060-07
69. Wolfgang M., van Putten J.P., Hayes S.F., Dorward D., and Koomey M. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 19 (2000) 6408-6418 10.1093/emboj/19.23.6408
70. Hwang J., Bieber D., Ramer S.W., Wu C.Y., Schoolnik, and G.K. Structural and topographical studies of the type IV bundle-forming pilus assembly complex of enteropathogenic Escherichia coli. J. Bacteriol. 185 (2003) 6695-6701
71. Daniel A., Singh A., Crowther L.J., Fernandes P.J., Schreiber W., and Donnenberg M.S. Interaction and localization studies of enteropathogenic Escherichia coli type IV bundle-forming pilus outer membrane components. Microbiology 152 (2006) 2405-2420 10.1099/mic.0.28860-0
72. Nunn D., Bergman S., and Lory S. Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J. Bacteriol. 172 (1990) 2911-2919
73. Arts J., de Groot A., Ball G., Durand E., Khattabi M.E., Filloux A., et al. Interaction domains in the Pseudomonas aeruginosa type II secretory apparatus component XcpS (GspF). Microbiology 153 (2007) 1582-1592 153/5/1582 [pii]; 10.1099/mic.0.2006/002840-0 [doi]
74. Koo J., Tammam S., Ku S.Y., Sampaleanu L.M., Burrows L.L., and Howell P.L. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin. J. Bacteriol. 190 (2008) 6961-6969 10.1128/JB.00996-08
75. Folster J.P., Dhulipala V., Nicholas R.A., and Shafer W.M. Differential regulation of ponA and pilMNOPQ expression by the MtrR transcriptional regulatory protein in Neisseria gonorrhoeae. J. Bacteriol. 189 (2007) 4569-4577 10.1128/JB.00286-07
76. Hoang T.T., Karkhoff-Schweizer R.R., Kutchma A.J., and Schweizer H.P. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212 (1998) 77-86
77. Salamitou S., Lemaire M., Fujino T., Ohayon H., Gounon P., Beguin P., and Aubert J.P. Subcellular localization of Clostridium thermocellum ORF3p, a protein carrying a receptor for the docking sequence borne by the catalytic components of the cellulosome. J. Bacteriol. 176 (1994) 2828-2834
78. Gallant C.V., Daniels C., Leung J.M., Ghosh A.S., Young K.D., Kotra L.P., and Burrows L.L. Common beta-lactamases inhibit bacterial biofilm formation. Mol. Microbiol. 58 (2005) 1012-1024. 10.1111/j.1365-2958.2005.04892.x
79. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with Image J. Biophotonics Int. 11 (2004) 36-42
80. 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 10.1128/JB.01224-06
81. Bradley D.E. Basic characterization of a Pseudomonas aeruginosa pilus-dependent bacteriophage with a long noncontractile tail. J. Virol. 12 (1973) 1139-1148
82. Watson A.A., Mattick J.S., and Alm R.A. Functional expression of heterologous type 4 fimbriae in Pseudomonas aeruginosa. Gene 175 (1996) 143-150
83. West S.E., Schweizer H.P., Dall C., Sample A.K., and Runyen-Janecky L.J. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148 (1994) 81-86