ExoS controls the cell contact-mediated switch to effector secretion in Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 190, Issue 8, 2008, Pages 2726-2738

  Cisz, Michelle ^a   Lee, Pei Chung ^a   Rietsch, Arne ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CARRIER PROTEIN; EXOENZYME S; GREEN FLUORESCENT PROTEIN; PROTEIN EXOT; PROTEIN EXOY; PROTEIN EXSE; PROTEIN PCRV; PROTEIN POPB; PROTEIN POPD; PROTEIN POPN; UNCLASSIFIED DRUG;

ARTICLE; CELL CONTACT; CELL SPECIFICITY; FEEDBACK SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; REPORTER GENE; TARGET CELL;

ADP RIBOSE TRANSFERASES; BACTERIAL TOXINS; CALCIUM; CELL LINE; EPITHELIAL CELLS; FEEDBACK, BIOCHEMICAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; YERSINIA;

EID: 41949093141     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01553-07     Document Type: Article

References (78)

1. Aili, M., E. L. Isaksson, S. E. Carlsson, H. Wolf-Watz, R. Rosqvist, and M. S. Francis. Regulation of Yersinia Yop-effector delivery by translocated YopE. Int J. Med. Microbiol., in press.
2. Aili, M., E. L. Isaksson, B. Hallberg, H. Wolf-Watz, and R. Rosqvist. 2006. Functional analysis of the YopE GTPase-activating protein (GAP) activity of Yersinia pseudotuberculosis. Cell. Microbiol. 8:1020-1033.
3. Barbieri, J. T., and J. Sun. 2004. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 152:79-92.
4. Bhakdi, S., H. Bayley, A. Valeva, I. Walev, B. Walker, M. Kehoe, and M. Palmer. 1996. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165:73-79.
5. Blaylock, B., K. E. Riordan, D. M. Missiakas, and O. Schneewind. 2006. Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL. J. Bacteriol. 188:3525-3534.
6. Bleves, S., C. Soscia, P. Nogueira-Orlandi, A. Lazdunski, and A. Filloux. 2005. Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J. Bacteriol. 187:3898-3902.
7. Broms, J. E., A. L. Forslund, A. Forsberg, and M. S. Francis. 2003. PcrH of Pseudomonas aeruginosa is essential for secretion and assembly of the type III translocon. J. Infect. Dis. 188:1909-1921.
8. Broz, P., C. A. Mueller, S. A. Muller, A. Philippsen, I. Sorg, A. Engel, and G. R. Cornelis. 2007. Function and molecular architecture of the Yersinia injectisome tip complex. Mol. Microbiol. 65:1311-1320.
9. Chastre, J., and J. Y. Fagon. 2002. Ventilator-associated pneumonia. Am. J. Respir. Crit. Care Med. 165:867-903.
10. Coburn, J., S. T. Dillon, B. H. Iglewski, and D. M. Gill. 1989. Exoenzyme S of Pseudomonas aeruginosa ADP-ribosylates the intermediate filament protein vimentin. Infect. Immun. 57:996-998.
11. Dacheux, D., J. Goure, J. Chabert, Y. Usson, and I. Attree. 2001. Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol. Microbiol. 40:76-85.
12. Dasgupta, N., G. L. Lykken, M. C. Wolfgang, and T. L. Yahr. 2004. A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 53:297-308.
13. Day, J. B., and G. V. Plano. 1998. A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol. Microbiol. 30:777-788.
14. DiNovo, A. A., K. L. Schey, W. S. Vachon, E. M. McGuffie, J. C. Olson, and T. S. Vincent. 2006. ADP-ribosylation of cyclophilin A by Pseudomonas aeruginosa exoenzyme S. Biochemistiy 45:4664-4673.
15. Edqvist, P. J., M. Aili, J. Liu, and M. S. Francis. 2007. Minimal YopB and YopD translocator secretion by Yersinia is sufficient for Yop-effector delivery into target cells. Microbes Infect. 9:224-233.
16. Espina, M., S. F. Ausar, C. R. Middaugh, M. A. Baxter, W. D. Picking, and W. L. Picking. 2007. Conformational stability and differential structural analysis of LcrV, PcrV, BipD, and SipD from type III secretion systems. Protein Sci. 16:704-714.
17. Faudry, E., G. Vernier, E. Neumann, V. Forge, and I. Attree. 2006. Synergistic pore formation by type III toxin translocators of Pseudomonas aeruginosa. Biochemistry 45:8117-8123.
18. Feltman, H., G. Schulert, S. Khan, M. Jain, L. Peterson, and A. R. Hauser. 2001. Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 147:2659-2669.
19. Ferracci, F., F. D. Schubot, D. S. Waugh, and G. V. Plano. 2005. Selection and characterization of Yersinia pestis YopN mutants that constitutively block Yop secretion. Mol. Microbiol. 57:970-987.
20. Fleiszig, S. M., T. S. Zaidi, M. J. Preston, M. Grout, D. J. Evans, and G. B. Pier. 1996. Relationship between cytotoxicity and corneal epithelial cell invasion by clinical isolates of Pseudomonas aeruginosa. Infect. Immun. 64:2288-2294.
21. Frank, D. W. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26:621-629.
22. Frank, D. W., and B. H. Iglewski. 1991. Cloning and sequence analysis of a irarts-regulatory locus required for exoenzyme S synthesis in Pseudomonas aeruginosa. J. Bacteriol. 173:6460-6468.
23. Fraylick, J. E., M. J. Riese, T. S. Vincent, J. T. Barbieri, and J. C. Olson. 2002. ADP-ribosylation and functional effects of Pseudomonas exoenzyme S on cellular RalA. Biochemistry 41:9680-9687.
24. Garau, J., and L. Gomez. 2003. Pseudomonas aeruginosa pneumonia. Curr. Opin. Infect. Dis. 16:135-143.
25. Goehring, U. M., G. Schmidt, K. J. Pederson, K. Aktories, and J. T. Barbieri. 1999. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 274:36369-36372.
26. Gonzalez-Pedrajo, B., G. M. Fraser, T. Minamino, and R. M. Macnab. 2002. Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Mol. Microbiol. 45:967-982.
27. Goure, J., P. Broz, O. Attree, G. R. Cornelis, and I. Attree. 2005. Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J. Infect. Dis. 192:218-225.
28. Goure, J., A. Pastor, E. Faudry, J. Chabert, A. Dessen, and I. Attree. 2004. The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect. Immun. 72:4741-4750.
29. Hauser, A. R., E. Cobb, M. Bodi, D. Mariscal, J. Valles, J. N. Engel, and J. Rello. 2002. Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit. Care Med. 30:521-528.
30. Hoang, T. T., A. J. Kutchma, A. Becher, and H. P. Schweizer. 2000. Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43:59-72.
31. Holder, I. A., A. N. Neely, and D. W. Frank. 2001. Type III secretion/intoxication system important in virulence of Pseudomonas aeruginosa infections in burns. Burns 27:129-130.
32. Holmstrom, A., J. Petterson, R. Rosqvist, S. Hakansson, F. Tafazoli, M. Fallman, K. E. Magnusson, H. Wolf-Watz, and A. Forsberg. 1997. YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol. Microbiol. 24:73-91.
33. Hornef, M. W., A. Roggenkamp, A. M. Geiger, M. Hogardt, C. A. Jacobi, and J. Heesemann. 2000. Triggering the ExoS regulon of Pseudomonas aeruginosa: a GFP-reporter analysis of exoenzyme (Exo) S, ExoT and ExoU synthesis. Microb. Pathog. 29:329-343.
34. Lee, V. T., D. M. Anderson, and O. Schneewind. 1998. Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone. Mol. Microbiol. 28:593-601.
35. Lee, V. T., S. K. Mazmanian, and O. Schneewind. 2001. A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J. Bacteriol. 183:4970-4978.
36. Lee, V. T., and O. Schneewind. 1999. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu. Mol. Microbiol. 31:1619-1629.
37. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
38. Maresso, A. W., M. R. Baldwin, and J. T. Barbieri. 2004. Ezrin/radixin/moesin proteins are high affinity targets for ADP-ribosylation by Pseudomonas aeruginosa ExoS. J. Biol. Chem. 279:38402-38408.
39. Marketon, M. M., R. W. DePaolo, K. L. DeBord, B. Jabri, and O. Schneewind. 2005. Plague bacteria target immune cells during infection. Science 309:1739-1741.
40. McCaw, M. L., G. L. Lykken, P. K. Singh, and T. L. Yahr. 2002. ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol. Microbiol. 46:1123-1133.
41. McGuffie, E. M., D. W. Frank, T. S. Vincent, and J. C. Olson. 1998. Modification of Ras in eukaryotic cells by Pseudomonas aeruginosa exoenzyme S. Infect. Immun. 66:2607-2613.
42. McGuffie, E. M., J. E. Fraylick, D. J. Hazen-Martin, T. S. Vincent, and J. C. Olson. 1999. Differential sensitivity of human epithelial cells to Pseudomonas aeruginosa exoenzyme S. Infect. Immun. 67:3494-3503.
43. Miyata, S., M. Casey, D. W. Frank, F. M. Ausubel, and E. Drenkard. 2003. Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71:2404-2413.
44. Mueller, C. A., P. Broz, S. A. Muller, P. Ringler, F. Erne-Brand, I. Sorg, M. Kuhn, A. Engel, and G. R. Cornelis. 2005. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310:674-676.
45. National Nosocomial Infections Surveillance System. 2004. National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am. J. Infect Control 32:470-485.
46. Nordfelth, R., and H. Wolf-Watz. 2001. YopB of Yersinia enterocolitica is essential for YopE translocation. Infect. Immun. 69:3516-3518.
47. Olive, A. J., R. Kenjale, M. Espina, D. S. Moore, W. L. Picking, and W. D. Picking. 2007. Bile salts stimulate recruitment of IpaB to the Shigella flexneri surface, where it colocalizes with IpaD at the tip of the type III secretion needle. Infect. Immun. 75:2626-2629.
48. Parsot, C., C. Hamiaux, and A. L. Page. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14.
49. Pirnay, J. P., D. De Vos, C. Cochez, F. Bilocq, J. Pirson, M. Struelens, L. Duinslaeger, P. Cornelis, M. Zizi, and A. Vanderkelen. 2003. Molecular epidemiology of Pseudomonas aeruginosa colonization in a burn unit: persistence of a multidrug-resistant clone and a silver sulfadiazine-resistant clone. J. Clin. Microbiol. 41:1192-1202.
50. Pukatzki, S., R. H. Kessin, and J. J. Mekalanos. 2002. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dicryostelium discoideum. Proc. Natl. Acad. Sci. USA 99:3159-3164.
51. Radke, J., K. J. Pederson, and J. T. Barbieri. 1999. Pseudomonas aeruginosa exoenzyme S is a biglutamic acid ADP-ribosyltransferase. Infect. Immun. 67:1508-1510.
52. Rahme, L. G., E. J. Stevens, S. F. Wolfort, J. Shao, R. G. Tompkins, and F. M. Ausubel. 1995. Common virulence factors for bacterial pathogenicity in plants and animals. Science 268:1899-1902.
53. Riese, M. J., A. Wittinghofer, and J. T. Barbieri. 2001. ADP ribosylation of Arg41 of Rap by ExoS inhibits the ability of Rap to interact with its guanine nucleotide exchange factor, C3G. Biochemistry. 40:3289-3294.
54. Rietsch, A., and J. J. Mekalanos. 2006. Metabolic regulation of type III secretion gene expression in Pseudomonas aeruginosa. Mol. Microbiol. 59:807-820.
55. Rietsch, A., I. Vallet-Gely, S. L. Dove, and J. J. Mekalanos. 2005. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 102:8006-8011.
56. Rietsch, A., M. C. Wolfgang, and J. J. Mekalanos. 2004. Effect of metabolic imbalance on expression of type III secretion genes in Pseudomonas aeruginosa. Infect. Immun. 72:1383-1390.
57. Rucks, E. A., and J. C. Olson. 2005. Characterization of an ExoS type III translocation-resistant cell line. Infect. Immun. 73:638-643.
58. Ryndak, M. B., H. Chung, E. London, and J. B. Bliska. 2005. Role of predicted transmembrane domains for type III translocation, pore formation, and signaling by the Yersinia pseudotuberculosis YopB protein. Infect. Immun. 73:2433-2443.
59. Sato, H., D. W. Frank, C. J. Hillard, J. B. Feix, R. R. Pankhaniya, K. Moriyama, V. Finck-Barbancon, A. Buchaklian, M. Lei, R. M. Long, J. Wiener-Kronish, and T. Sawa. 2003. The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J. 22:2959-2969.
60. Schlumberger, M. C., A. J. Muller, K. Ehrbar, B. Winnen, I. Duss, B. Stecher, and W. D. Hardt. 2005. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc. Natl. Acad. Sci. USA 102:12548-12553.
61. Schoehn, G., A. M. Di Guilmi, D. Lemaire, I. Attree, W. Weissenhorn, and A. Dessen. 2003. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J. 22:4957-4967.
62. Sorg, I., S. Wagner, M. Amstutz, S. A. Muller, P. Broz, Y. Lussi, A. Engel, and G. R. Cornelis. 2007. YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J. 26:3015-3024.
63. Sun, J., and J. T. Barbieri. 2003. Pseudomonas aeruginosa ExoT ADP-ribosylates CT10 regulator of kinase (Crk) proteins. J. Biol. Chem. 278:32794-32800.
64. Sundin, C., J. Thelaus, J. E. Broms, and K. Forsberg. 2004. Polarisation of type III translocation by Pseudomonas aeruginosa requires PcrG, PcrV and PopN. Microb. Pathog. 37:313-322.
65. Sundin, C., M. C. Wolfgang, S. Lory, A. Forsberg, and E. Frithz-Lindsten. 2002. Type IV pili are not specifically required for contact dependent translocation of exoenzymes by Pseudomonas aeruginosa. Microb. Pathog. 33:265-277.
66. Torruellas, J., M. W. Jackson, J. W. Pennock, and G. V. Plano. 2005. The Yersinia pestis type III secretion needle plays a role in the regulation of Yop secretion. Mol. Microbiol. 57:1719-1733.
67. Urbanowski, M. L., E. D. Brutinel, and T. L. Yahr. 2007. Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 75:4432-4439.
68. Urbanowski, M. L., G. L. Lykken, and T. L. Yahr. 2005. A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc. Natl. Acad. Sci. USA 102:9930-9935.
69. Vallis, A. J., T. L. Yahr, J. T. Barbieri, and D. W. Frank. 1999. Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions. Infect. Immun. 67:914-920.
70. Vance, R. E., A. Rietsch, and J. J. Mekalanos. 2005. Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect. Immun. 73:1706-1713.
71. Veenendaal, A. K., J. L. Hodgkinson, L. Schwarzer, D. Stabat, S. F. Zenk, and A. J. Blocker. 2007. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol. Microbiol. 63:1719-1730.
72. Viboud, G. I., and J. B. Bliska. 2001. A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20:5373-5382.
73. Warrens, A. N., M. D. Jones, and R. I. Lechler. 1997. Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest. Gene 186:29-35.
74. Wolfgang, M. C., V. T. Lee, M. E. Gilmore, and S. Lory. 2003. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell 4:253-263.
75. Yahr, T. L., L. M. Mende-Mueller, M. B. Friese, and D. W. Frank. 1997. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 179:7165-7168.
76. Yahr, T. L., A. J. Vallis, M. K. Hancock, J. T. Barbieri, and D. W. Frank. 1998. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. USA 95:13899-13904.
77. Zhang, Y., Q. Deng, J. A. Porath, C. L. Williams, K. J. Pederson-Gulrud, and J. T. Barbieri. 2007. Plasma membrane localization affects the RhoGAP specificity of Pseudomonas ExoS. Cell. Microbiol. 9:2192-2201.
78. Zheng, Z., G. Chen, S. Joshi, E. D. Brutinel, T. L. Yahr, and L. Chen. 2007. Biochemical characterization of a regulatory cascade controlling transcription of the Pseudomonas aeruginosa type III secretion system. J. Biol. Chem. 282:6136-6142.