Protein secretion systems in Pseudomonas aeruginosa: A wealth of pathogenic weapons

International Journal of Medical Microbiology

Volumn 300, Issue 8, 2010, Pages 534-543

  Bleves, Sophie ^a   Viarre, Véronique ^a   Salacha, Richard ^a   Michel, Gérard P F ^a   Filloux, Alain ^b   Voulhoux, Romé ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Gram negative bacteria; Pathogenicity; Protein secretion systems; Pseudomonas aeruginosa; Secretome

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; CHAPERONE;

BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; HOST PATHOGEN INTERACTION; NONHUMAN; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; SHORT SURVEY; TRANSCRIPTION REGULATION; TYPE I SECRETION SYSTEM; TYPE II SECRETION SYSTEM; TYPE III SECRETION SYSTEM; TYPE V SECRETION SYSTEM; TYPE VI SECRETION SYSTEM;

EID: 78549236798     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2010.08.005     Document Type: Short Survey

References (135)

1. Abdallah A.M., Verboom T., Weerdenburg E.M., Gey van Pittius N.C., Mahasha P.W., Jimenez C., Parra M., Cadieux N., Brennan M.J., Appelmelk B.J., Bitter W. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol. Microbiol. 2009, 73:329-340.
2. Alcorn J.F., Wright J.R. Degradation of pulmonary surfactant protein D by Pseudomonas aeruginosa elastase abrogates innate immune function. J. Biol. Chem. 2004, 279:30871-30879.
3. Allured V.S., Collier R.J., Carroll S.F., McKay D.B. Structure of exotoxin A of Pseudomonas aeruginosa at 3.0-angstrom resolution. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:1320-1324.
4. Alphonse S., Durand E., Douzi B., Waegele B., Darbon H., Filloux A., Voulhoux R., Bernard C. Structure of the Pseudomonas aeruginosa XcpT pseudopilin, a major component of the type II secretion system. J. Struct. Biol. 2010, 169:75-80.
5. Arts J., van Boxtel R., Filloux A., Tommassen J., Koster M. Export of the pseudopilin XcpT of the Pseudomonas aeruginosa type II secretion system via the signal recognition particle-Sec pathway. J. Bacteriol. 2007, 189:2069-2076.
6. Aschtgen M.S., Bernard C.S., De Bentzmann S., Lloubes R., Cascales E. J. Bacteriol. 2008, 190:7523-7531.
7. Ball G., Durand E., Lazdunski A., Filloux A. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 2002, 43:475-485.
8. Ballister E.R., Lai A.H., Zuckermann R.N., Cheng Y., Mougous J.D. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3733-3738.
9. Barbieri J.T., Sun J. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 2004, 152:79-92.
10. Barker A.P., Vasil A.I., Filloux A., Ball G., Wilderman P.J., Vasil M.L. A novel extracellular phospholipase C of Pseudomonas aeruginosa is required for phospholipid chemotaxis. Mol. Microbiol. 2004, 53:1089-1098.
11. Bendtsen J.D., Wooldridge K.G. Non-classical secretion. Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis 2009, 225-235. Caister Academic Press, Norfolk. K.G. Wooldridge (Ed.).
12. Binet R., Letoffe S., Ghigo J.M., Delepelaire P., Wandersman C. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene 1997, 192:7-11.
13. Bingle L.E., Bailey C.M., Pallen M.J. Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 2008, 11:3-8.
14. Bleves S., Lazdunski A., Filloux A. Membrane topology of three Xcp proteins involved in exoprotein transport by Pseudomonas aeruginosa. J. Bacteriol. 1996, 178:4297-4300.
15. Bleves S., Soscia C., Nogueira-Orlandi P., Lazdunski A., Filloux A. Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J. Bacteriol. 2005, 187:3898-3902.
16. Bonemann G., Pietrosiuk A., Diemand A., Zentgraf H., Mogk A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 2009, 28:315-325.
17. Borlee B.R., Goldman A.D., Murakami K., Samudrala R., Wozniak D.J., Parsek M.R. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol. Microbiol. 2010, 75:827-842.
18. Braun P., de Groot A., Bitter W., Tommassen J. Secretion of elastinolytic enzymes and their propeptides by Pseudomonas aeruginosa. J. Bacteriol. 1998, 180:3467-3469.
19. Cahan R., Axelrad I., Safrin M., Ohman D.E., Kessler E. A secreted aminopeptidase of Pseudomonas aeruginosa. Identification, primary structure, and relationship to other aminopeptidases. J. Biol. Chem. 2001, 276:43645-43652.
20. Chapon-Herve V., Akrim M., Latifi A., Williams P., Lazdunski A., Bally M. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol. Microbiol. 1997, 24:1169-1178.
21. Clantin B., Hodak H., Willery E., Locht C., Jacob-Dubuisson F., Villeret V. The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl. Acad. Sci. USA 2004, 1:6194-6199.
22. Clantin B., Delattre A.S., Rucktooa P., Saint N., Méli A.C., Locht C., Jacob-Dubuisson F., Villeret V. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 2007, 17:957-991.
23. Cornelis G.R. The type III secretion injectisome. Nat. Rev. Microbiol. 2006, 4:811-825.
24. Coutte L., Willery E., Antoine R., Drobecq H., Locht C., Jacob-Dubuisson F. Surface anchoring of bacterial subtilisin important for maturation function. Mol. Microbiol. 2003, 49:529-539.
25. Dacheux D., Goure J., Chabert J., Usson Y., Attree I. Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol. Microbiol. 2001, 40:76-85.
26. Dasgupta N., Lykken G.L., Wolfgang M.C., Yahr T.L. A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 2004, 53:297-308.
27. Dautin N., Bernstein H.D. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 2007, 61:89-112.
28. De Bentzmann S., Polette M., Zahm J.M., Hinnrasky J., Kileztky C., Bajolet O., Klossek J.M., Filloux A., Lazdunski A., Puchelle E. Pseudomonas aeruginosa virulence factors delay airway epithelial wound repair by altering the actin cytoskeleton and inducing overactivation of epithelial matrix metalloproteinase-2. Lab. Invest. 2000, 80:209-219.
29. Delepelaire P. Type I secretion in Gram-negative bacteria. Biochim. Biophys. Acta 2004, 1694:149-161.
30. Douzi B., Durand E., Bernard C., Alphonse S., Cambillau C., Filloux A., Tegoni M., Voulhoux R. The XcpV/GspI pseudopilin has a central role in the assembly of a quaternary complex within the T2SS pseudopilus. J. Biol. Chem. 2009, 284:34580-34589.
31. Duong F., Lazdunski A., Murgier M. Protein secretion by heterologous bacterial ABC-transporters: the C-terminus secretion signal of the secreted protein confers high recognition specificity. Mol. Microbiol. 1996, 21:459-470.
32. Duong F., Bonnet E., Geli V., Lazdunski A., Murgier M., Filloux A. The AprX protein of Pseudomonas aeruginosa: a new substrate for the Apr type I secretion system. Gene 2001, 262:147-153.
33. Durand E., Bernadac A., Ball G., Lazdunski A., Sturgis J.N., Filloux A. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 2003, 185:2749-2758.
34. Durand E., Michel G., Voulhoux R., Kurner J., Bernadac A., Filloux A. XcpX controls biogenesis of the Pseudomonas aeruginosa XcpT-containing pseudopilus. J. Biol. Chem. 2005, 280:31378-31389.
35. Economou A., Christie P.J., Fernandez R.C., Palmer T., Plano G.V., Pugsley A.P. Secretion by numbers: protein traffic in prokaryotes. Mol. Microbiol. 2006, 62:308-319.
36. Engel J., Balachandran P. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 2009, 12:61-66.
37. Engel L.S., Hill J.M., Caballero A.R., Green L.C., O'Callaghan R.J. Protease IV, a unique extracellular protease and virulence factor from Pseudomonas aeruginosa. J. Biol. Chem. 1998, 273:16792-16797.
38. Filloux A. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 2004, 1694:163-179.
39. Filloux A. The type VI secretion system: a tubular story. EMBO J. 2009, 28:309-310.
40. Filloux A., Bally M., Soscia C., Murgier M., Lazdunski A. Phosphate regulation in Pseudomonas aeruginosa: cloning of the alkaline phosphatase gene and identification of phoB- and phoR-like genes. Mol. Gen. Genet. 1988, 212:510-513.
41. Filloux A., Bleves S., van Ulsen P., Tommassen J. Protein secretion mechanisms in Pseudomonas. Pseudomonas, vol. I. Genomics, Life Style and Molecular Architecture 2003, 749-792. Kluwer Academic/Plenum Publishers, New York. J.-L. Ramos (Ed.).
42. Filloux A., Hachani A., Bleves S. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 2008, 154:1570-1583.
43. Finck-Barbancon V., Yahr T.L., Frank D.W. Identification and characterization of SpcU, a chaperone required for efficient secretion of the ExoU cytotoxin. J. Bacteriol. 1998, 180:6224-6231.
44. Folders J., Tommassen J., van Loon L.C., Bitter W. Identification of a chitin-binding protein secreted by Pseudomonas aeruginosa. J. Bacteriol. 2000, 182:1257-1263.
45. Fox A., Haas D., Reimmann C., Heeb S., Filloux A., Voulhoux R. Emergence of secretion-defective sublines of Pseudomonas aeruginosa PAO1 resulting from spontaneous mutations in the vfr global regulatory gene. Appl. Environ. Microbiol. 2008, 74:1902-1908.
46. Frank D.W. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 1997, 26:621-629.
47. Gerard-Vincent M., Robert V., Ball G., Bleves S., Michel G.P., Lazdunski A., Filloux A. Identification of XcpP domains that confer functionality and specificity to the Pseudomonas aeruginosa type II secretion apparatus. Mol. Microbiol. 2002, 44:1651-1665.
48. Goodman A.L., Kulasekara B., Rietsch A., Boyd D., Smith R.S., Lory S. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 2004, 7:745-754.
49. Goure J., Pastor A., Faudry E., Chabert J., Dessen A., Attree I. The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect. Immun. 2004, 72:4741-4750.
50. Guzzo J., Pages J.M., Duong F., Lazdunski A., Murgier M. Pseudomonas aeruginosa alkaline protease: evidence for secretion genes and study of secretion mechanism. J. Bacteriol. 1991, 173:5290-5297.
51. Hauser A.R. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat. Rev. Microbiol. 2009, 7:654-665.
52. Henderson I.R., Navarro-Garcia F., Desvaux M., Fernandez R.C., Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 2004, 68:692-744.
53. Hendrixson D.R., de la Morena M.L., Stathopoulos C., St Geme J.W. Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol. Microbiol. 1997, 26:505-518.
54. Hodak H., Jacob-Dubuisson F. Current challenges in autotransport and two-partner protein secretion pathways. Res. Microbiol. 2007, 158:631-637.
55. Hogardt M., Roeder M., Schreff A.M., Eberl L., Heesemann J. Expression of Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology 2004, 150:843-851.
56. Holland I.B., Schmitt L., Young J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol. Membr. Biol. 2005, 22:29-39.
57. Hood R.D., Singh P., Hsu F., Guvener T., Carl M.A., Trinidad R.R., Silverman J.M., Ohlson B.B., Hicks K.G., Plemel R.L., Li M., Schwarz S., Wang W.Y., Merz A.J., Goodlett D.R., Mougous J.D. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010, 7:25-37.
58. Hornef M.W., Roggenkamp A., Geiger A.M., Hogardt M., Jacobi C.A., Heesemann J. Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb. Pathog. 2000, 29:329-343.
59. Hsu F., Schwarz S., Mougous J.D. TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol. Microbiol. 2009, 72:1111-1125.
60. Jacob-Dubuisson F., Locht C., Antoine R. Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 2001, 40:306-313.
61. Jaeger K.E., Ransac S., Dijkstra B.W., Colson C., van Heuvel M., Misset O. Bacterial lipases. FEMS Microbiol. Rev. 1994, 15:29-63.
62. Journet L., Agrain C., Broz P., Cornelis G.R. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 2003, 302:1757-1760.
63. Kanamaru S., Leiman P.G., Kostyuchenko V.A., Chipman P.R., Mesyanzhinov V.V., Arisaka F., Rossmann M.G. Structure of the cell-puncturing device of bacteriophage T4. Nature 2002, 415:553-557.
64. Kida Y., Higashimoto Y., Inoue H., Shimizu T., Kuwano K. A novel secreted protease from Pseudomonas aeruginosa activates NF-kappaB through protease-activated receptors. Cell. Microbiol. 2008, 10:1491-1504.
65. Kipnis E., Sawa T., Wiener-Kronish J. Targeting mechanisms of Pseudomonas aeruginosa pathogenesis. Med. Mal. Infect. 2006, 36:78-91.
66. Köhler R., Schäfer K., Müller S., Vignon G., Diederichs K., Philippsen A., Ringler P., Pugsley A.P., Engel A., Welte W. Structure and assembly of the pseudopilin PulG. Mol. Microbiol. 2004, 54:647-664.
67. Kon Y., Tsukada H., Hasegawa T., Igarashi K., Wada K., Suzuki E., Arakawa M., Gejyo F. The role of Pseudomonas aeruginosa elastase as a potent inflammatory factor in a rat air pouch inflammation model. FEMS Immunol. Med. Microbiol. 1999, 25:313-321.
68. Koronakis V., Sharff A., Koronakis E., Luisi B., Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 2000, 405:914-919.
69. Korotkov K.V., Hol W.G. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat. Struct. Mol. Biol. 2008, 15:462-468.
70. Koster M., Bitter W., de Cock H., Allaoui A., Cornelis G.R., Tommassen J. The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol. Microbiol. 1997, 26:789-797.
71. Kulasekara B.R., Kulasekara H.D., Wolfgang M.C., Stevens L., Frank D.W., Lory S. Acquisition and evolution of the exoU locus in Pseudomonas aeruginosa. J. Bacteriol. 2006, 188:4037-4050.
72. Lazdunski A.M., Ventre I., Sturgis J.N. Regulatory circuits and communication in Gram-negative bacteria. Nat. Rev. Microbiol. 2004, 2:581-592.
73. Leiman P.G., Basler M., Ramagopal U.A., Bonanno J.B., Sauder J.M., Pukatzki S., Burley S.K., Almo S.C., Mekalanos J.J. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4154-4159.
74. Lesic B., Starkey M., He J., Hazan R., Rahme L.G. Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 2009, 155:2845-2855.
75. Letoffe S., Redeker V., Wandersman C. Isolation and characterization of an extracellular haem-binding protein from Pseudomonas aeruginosa that shares function and sequence similarities with the Serratia marcescens HasA haemophore. Mol. Microbiol. 1998, 28:1223-1234.
76. Letzelter M., Sorg I., Mota L.J., Meyer S., Stalder J., Feldman M., Kuhn M., Callebaut I., Cornelis G.R. The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J. 2006, 25:3223-3233.
77. Linke D., Riess T., Autenrieth I.B., Lupas A., Kempf V.A. Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 2006, 14:264-270.
78. Llamas M.A., van der Sar A., Chu B.C., Sparrius M., Vogel H.J., Bitter W. A novel extracytoplasmic function (ECF) sigma factor regulates virulence in Pseudomonas aeruginosa. PLoS Pathog. 2009, 5(9):e1000572. Epub 2009 September 4.
79. Lu H.M., Mizushima S., Lory S. A periplasmic intermediate in the extracellular secretion pathway of Pseudomonas aeruginosa exotoxin A. J. Bacteriol. 1993, 175:7463-7467.
80. Ma Q., Zhai Y., Schneider J.C., Ramseier T.M., Saier M.H. Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim. Biophys. Acta 2003, 1611:223-233.
81. Ma A.T., McAuley S., Pukatzki S., Mekalanos J.J. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 2009, 5:234-243.
82. Martinez A., Ostrovsky P., Nunn D.N. LipC, a second lipase of Pseudomonas aeruginosa, is LipB and Xcp dependent and is transcriptionally regulated by pilus biogenesis components. Mol. Microbiol. 1999, 34:317-326.
83. Matsumoto K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol. Chem. 2004, 385:1007-1016.
84. Mazar J., Cotter P.A. New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol. 2007, 15:508-515.
85. McCaw M.L., Lykken G.L., Singh P.K., Yahr T.L. ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol. Microbiol. 2002, 46:1123-1133.
86. Michel G.P., Voulhoux R. The type II secretory system (T2SS) in Gram-negative bacteria: a molecular nanomachine for secretion of Sec and Tat-dependent extracellular proteins. Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis 2009, 67-92. Caister Academic Press, Norfolk. K.G. Wooldridge (Ed.).
87. Michel G.P., Durand E., Filloux A. XphA/XqhA, a novel GspCD subunit for type II secretion in Pseudomonas aeruginosa. J. Bacteriol. 2007, 189:3776-3783.
88. Mougous J.D., Cuff M.E., Raunser S., Shen A., Zhou M., Gifford C.A., Goodman A.L., Joachimiak G., Ordonez C.L., Lory S., Walz T., Joachimiak A., Mekalanos J.J. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006, 312:1526-1530.
89. Mougous J.D., Gifford C.A., Ramsdell T.L., Mekalanos J.J. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 2007, 9:797-803.
90. Mueller C.A., Broz P., Müller S.A., Ringler P., Erne-Brand F., Sorg I., Kuhn M., Engel A., Cornelis G.R. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 2005, 310:674-676.
91. Mulcahy H., O'Callaghan J., O'Grady E.P., Adams C., O'Gara F. The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect. Immun. 2006, 74:3012-3015.
92. Nummelin H., Merckel M.C., Leo J.C., Lankinen H., Skurnik M., Goldman A. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO J. 2004, 23:701-711.
93. Olson J.C., Ohman D.E. Efficient production and processing of elastase and LasA by Pseudomonas aeruginosa require zinc and calcium ions. J. Bacteriol. 1992, 174:4140-4147.
94. Oomen C.J., van Ulsen P., van Gelder P., Feijen M., Tommassen J., Gros P. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 2004, 23:1257-1266.
95. Ostroff R.M., Vasil A.I., Vasil M.L. Molecular comparison of a nonhemolytic and a hemolytic phospholipase C from Pseudomonas aeruginosa. J. Bacteriol. 1990, 172:5915-5923.
96. Pastor A., Chabert J., Louwagie M., Garin J., Attree I. PscF is a major component of the Pseudomonas aeruginosa type III secretion needle. FEMS Microbiol. Lett. 2005, 253:95-101.
97. Peabody C.R., Chung Y.J., Yen M.R., Vidal-Ingigliardi D., Pugsley A.P., Saier M.H. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 2003, 149:3051-3072.
98. Potvin E., Lehoux D.E., Kukavica-Ibrulj I., Richard K.L., Sanschagrin F., Lau G.W., Levesque R.C. In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ. Microbiol. 2003, 5:1294-1308.
99. Pukatzki S., Ma A.T., Sturtevant D., Krastins B., Sarracino D., Nelson W.C., Heidelberg J.F., Mekalanos J.J. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1528-1533.
100. Pukatzki S., Ma A.T., Revel A.T., Sturtevant D., Mekalanos J.J. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15508-15513.
101. Pukatzki S., McAuley S.B., Miyata S.T. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 2009, 12:11-17.
102. Quinaud M., Chabert J., Faudry E., Neumann E., Lemaire D., Pastor A., Elsen S., Dessen A., Attree I. The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa. J. Biol. Chem. 2005, 280:36293-36300.
103. Rietsch A., Vallet-Gely I., Dove S.L., Mekalanos J.J. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8006-8011.
104. Robert V., Filloux A., Michel G.P. Subcomplexes from the Xcp secretion system of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 2005, 252:43-50.
105. Robert V., Filloux A., Michel G.P. Role of XcpP in the functionality of the Pseudomonas aeruginosa secreton. Res. Microbiol. 2005, 156:880-886.
106. Ruer S., Stender S., Filloux A., de Bentzmann S. Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J. Bacteriol. 2007, 189:3547-3555.
107. Ruer S., Ball G., Filloux A., de Bentzmann S. The 'P-usher', a novel protein transporter involved in fimbrial assembly and TpsA secretion. EMBO J. 2008, 27:2669-2680.
108. Salacha R., Kovacic F., Brochier-Armanet C., Wilhelm S., Tommassen J., Filloux A., Voulhoux R., Bleves S. The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel type V secretion system. Environ. Microbiol. 2010, 12:1498-1512.
109. Sato H., Frank D.W. ExoU is a potent intracellular phospholipase. Mol. Microbiol. 2004, 53:1279-1290.
110. Sauvonnet N., Vignon G., Pugsley A.P., Gounon P. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 2000, 19:2221-2228.
111. Sawa T., Yahr T.L., Ohara M., Kurahashi K., Gropper M.A., Wiener-Kronish J.P., Frank D.W. Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat. Med. 1999, 5:392-398.
112. Schoehn G., Di Guilmi A.M., Lemaire D., Attree I., Weissenhorn W., Dessen A. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J. 2003, 22:4957-4967.
113. Shen D.K., Quenee L., Bonnet M., Kuhn L., Derouazi M., Lamotte D., Toussaint B., Polack B. Orf1/SpcS chaperones ExoS for type three secretion by Pseudomonas aeruginosa. Biomed. Environ. Sci. 2008, 21:103-109.
114. Shere K.D., Sallustio S., Manessis A., D'Aversa T.G., Goldberg M.B. Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol. Microbiol. 1997, 25:451-462.
115. Soscia C., Hachani A., Bernadac A., Filloux A., Bleves S. Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J. Bacteriol. 2007, 189:3124-3132.
116. Stover C.K., Pham X.Q., Erwin A.L., Mizoguchi S.D., Warrener P., Hickey M.J., Brinkman F.S., Hufnagle W.O., Kowalik D.J., Lagrou M., Garber R.L., Goltry L., Tolentino E., Westbrock-Wadman S., Yuan Y., Brody L.L., Coulter S.N., Folger K.R., Kas A., Larbig K., Lim R., Smith K., Spencer D., Wong G.K., Wu Z., Paulsen I.T., Reizer J., Saier M.H., Hancock R.E., Lory S., Olson M.V. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000, 406:959-964.
117. Stuer W., Jaeger K.E., Winkler U.K. Purification of extracellular lipase from Pseudomonas aeruginosa. J. Bacteriol. 1986, 168:1070-1074.
118. Surana N.K., Cutter D., Barenkamp S.J., Geme St.J.W. The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J. Biol. Chem. 2004, 279:14679-14685.
119. Urbanowski M.L., Lykken G.L., Yahr T.L. A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9930-9935.
120. Urbanowski M.L., Brutinel E.D., Yahr T.L. Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 2007, 75:4432-4439.
121. van Ulsen P., van Alphen L., ten Hove J., Fransen F., van der Ley P., Tommassen J. A neisserial autotransporter NalP modulating the processing of other autotransporters. Mol. Microbiol. 2003, 50:1017-1030.
122. Ventre I., Goodman A.L., Vallet-Gely I., Vasseur P., Soscia C., Molin S., Bleves S., Lazdunski A., Lory S., Filloux A. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:171-176.
123. Voulhoux R., Tommassen J. Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res. Microbiol. 2004, 155:129-135.
124. Voulhoux R., Taupiac M.P., Czjzek M., Beaumelle B., Filloux A. Influence of deletions within domain II of exotoxin A on its extracellular secretion from Pseudomonas aeruginosa. J. Bacteriol. 2000, 182:4051-4058.
125. Voulhoux R., Ball G., Ize B., Vasil M.L., Lazdunski A., Wu L.F., Filloux A. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 2001, 20:6735-6741.
126. Wandersman C., Delepelaire P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 2004, 58:611-647.
127. Wilhelm S., Tommassen J., Jaeger K.E. A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J. Bacteriol. 1999, 181:6977-6986.
128. Wilhelm S., Gdynia A., Tielen P., Rosenau F., Jaeger K.E. The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation. J. Bacteriol. 2007, 189:6695-6703.
129. Woestyn S., Allaoui A., Wattiau P., Cornelis G.R. YscN, the putative energizer of the Yersinia Yop secretion machinery. J. Bacteriol. 1994, 176:1561-1569.
130. Wolfgang M.C., Kulasekara B.R., Liang X., Boyd D., Wu K., Yang Q., Miyada C.G., Lory S. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:8484-8489.
131. Yahr T.L., Wolfgang M.C. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 2006, 62:631-640.
132. Yahr T.L., Mende-Mueller L.M., Friese M.B., Frank D.W. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 1997, 179:7165-7168.
133. Yahr T.L., Vallis A.J., Hancock M.K., Barbieri J.T., Frank D.W. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13899-13904.
134. Yen M.R., Peabody C.R., Partovi S.M., Zhai Y., Tseng Y.H., Saier M.H. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim. Biophys. Acta 2002, 1562:6-31.
135. Yeo H.J., Cotter S.E., Laarmann S., Juehne T., St.Geme J.W., Waksman G. Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. EMBO J. 2004, 23:1245-1256.