Translocon-independent intracellular replication by Pseudomonas aeruginosa requires the ADP-ribosylation domain of ExoS

Microbes and Infection

Volumn 14, Issue 15, 2012, Pages 1366-1373

  Hritonenko, Victoria ^a   Evans, David J ^a,b   Fleiszig, Suzanne M J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TOURO UNIVERSITY CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ADPr domain; Epithelial cells; ExoS; Intracellular replication; Pseudomonas aeruginosa; Translocon; Vacuole

Indexed keywords

EXOS PROTEIN; EXOT PROTEIN; EXOY PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CELL VACUOLE; HUMAN; HUMAN CELL; INTRACELLULAR REPLICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA;

ADP RIBOSE TRANSFERASES; ANALYSIS OF VARIANCE; BACTERIAL TOXINS; BACTERIAL TRANSLOCATION; CELL LINE; CELL SHAPE; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; MICROSCOPY, PHASE-CONTRAST; PSEUDOMONAS AERUGINOSA; VACUOLES;

PSEUDOMONAS AERUGINOSA;

EID: 84870799980     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2012.08.007     Document Type: Article

References (42)

1. Eber M.R., Shardell M., Schweizer M.L., Laxminarayan R., Perencevich E.N. Seasonal and temperature-associated increases in gram-negative bacterial bloodstream infections among hospitalized patients. PLoS One 2011, 6:e25298.
2. Sandiumenge A., Rello J. Ventilator-associated pneumonia caused by ESKAPE organisms: cause, clinical features, and management. Curr. Opin. Pulm. Med. 2012, 18:187-193.
3. Stapleton F., Carnt N. Contact lens-related microbial keratitis: how have epidemiology and genetics helped us with pathogenesis and prophylaxis. Eye (London) 2012, 26:185-193.
4. McColley S.A., Ren C.L., Schechter M.S., Regelmann W.E., Pasta D.J., Konstan M.W. Risk factors for onset of persistent respiratory symptoms in children with cystic fibrosis. Pediatr. Pulmonol. 2012, 10.1002/ppul.22519.
5. Breidenstein E.B., de la Fuente-Nunez C., Hancock R.E. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 2011, 19:419-426.
6. Mathee K., Narasimhan G., Valdes C., Qiu X., Matewish J.M., Koehrsen M., Rokas A., Yandava C.N., Engels R., Zeng E., Olavarietta R., Doud M., Smith R.S., Montgomery P., White J.R., Godfrey P.A., Kodira C., Birren B., Galagan J.E., Lory S. Dynamics of Pseudomonas aeruginosa genome evolution. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3100-3105.
7. Hauser A.R. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat. Rev. Microbiol. 2009, 7:654-665.
8. Engel J., Balachandran P. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 2009, 12:61-66.
9. Fleiszig S.M., Wiener-Kronish J.P., Miyazaki H., Vallas V., Mostov K.E., Kanada D., Sawa T., Yen T.S., Frank D.W. Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 1997, 65:579-586.
10. Lee E.J., Cowell B.A., Evans D.J., Fleiszig S.M. Contribution of ExsA-regulated factors to corneal infection by cytotoxic and invasive Pseudomonas aeruginosa in a murine scarification model. Invest. Ophthalmol. Vis. Sci. 2003, 44:3892-3898.
11. Vance R.E., Rietsch A., Mekalanos J.J. Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect. Immun. 2005, 73:1706-1713.
12. 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.
13. Pederson K.J., Krall R., Riese M.J., Barbieri J.T. Intracellular localization modulates targeting of ExoS, a type III cytotoxin, to eukaryotic signalling proteins. Mol. Microbiol. 2002, 46:1381-1390.
14. Barbieri J.T., Sun J. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 2004, 152:79-92.
15. Anderson D.M., Schmalzer K.M., Sato H., Casey M., Terhune S.S., Haas A.L., Feix J.B., Frank D.W. Ubiquitin and ubiquitin-modified proteins activate the Pseudomonas aeruginosa T3SS cytotoxin, ExoU. Mol. Microbiol. 2011, 82:1454-1467.
16. Zolfaghar I., Evans D.J., Ronaghi R., Fleiszig S.M. Type III secretion-dependent modulation of innate immunity as one of multiple factors regulated by Pseudomonas aeruginosa RetS. Infect. Immun. 2006, 74:3880-3889.
17. Feltman H., Schulert G., Khan S., Jain M., Peterson L., Hauser A.R. Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 2001, 147:2659-2669.
18. Zhu H., Conibear T.C., Bandara R., Aliwarga Y., Stapleton F., Willcox M.D. Type III secretion system-associated toxins, proteases, serotypes, and antibiotic resistance of Pseudomonas aeruginosa isolates associated with keratitis. Curr. Eye Res. 2006, 31:297-306.
19. Shaver C.M., Hauser A.R. Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect. Immun. 2004, 72:6969-6977.
20. Lee V.T., Smith R.S., Tummler B., Lory S. Activities of Pseudomonas aeruginosa effectors secreted by the Type III secretion system in vitro and during infection. Infect. Immun. 2005, 73:1695-1705.
21. Miyata S., Casey M., Frank D.W., Ausubel F.M., Drenkard E. 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. 2003, 71:2404-2413.
22. Angus A.A., Lee A.A., Augustin D.K., Lee E.J., Evans D.J., Fleiszig S.M. Pseudomonas aeruginosa induces membrane blebs in epithelial cells, which are utilized as a niche for intracellular replication and motility. Infect. Immun. 2008, 76:1992-2001.
23. Angus A.A., Evans D.J., Barbieri J.T., Fleiszig S.M. The ADP-ribosylation domain of Pseudomonas aeruginosa ExoS is required for membrane bleb niche formation and bacterial survival within epithelial cells. Infect. Immun. 2010, 78:4500-4510.
24. Hritonenko V., Mun J.J., Tam C., Simon N.C., Barbieri J.T., Evans D.J., Fleiszig S.M. Adenylate cyclase activity of Pseudomonas aeruginosa ExoY can mediate bleb-niche formation in epithelial cells and contributes to virulence. Microb. Pathog. 2011, 51:305-312.
25. Makin S.A., Beveridge T.J. Pseudomonas aeruginosa PAO1 ceases to express serotype-specific lipopolysaccharide at 45 degrees C. J. Bacteriol. 1996, 178:3350-3352.
26. Cisz M., Lee P.C., Rietsch A. ExoS controls the cell contact-mediated switch to effector secretion in Pseudomonas aeruginosa. J. Bacteriol. 2008, 190:2726-2738.
27. Robertson D.M., Li L., Fisher S., Pearce V.P., Shay J.W., Wright W.E., Cavanagh H.D., Jester J.V. Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Invest. Ophthalmol. Vis. Sci. 2005, 46:470-478.
28. Masters S.C., Pederson K.J., Zhang L., Barbieri J.T., Fu H. Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. Biochemistry 1999, 38:5216-5221.
29. Maresso A.W., Deng Q., Pereckas M.S., Wakim B.T., Barbieri J.T. Pseudomonas aeruginosa ExoS ADP-ribosyltransferase inhibits ERM phosphorylation. Cell. Microbiol. 2007, 9:97-105.
30. Ganesan A.K., Frank D.W., Misra R.P., Schmidt G., Barbieri J.T. Pseudomonas aeruginosa exoenzyme S ADP-ribosylates Ras at multiple sites. J. Biol. Chem. 1998, 273:7332-7337.
31. Zhang L., Wang H., Masters S.C., Wang B., Barbieri J.T., Fu H. Residues of 14-3-3 zeta required for activation of exoenzyme S of Pseudomonas aeruginosa. Biochemistry 1999, 38:12159-12164.
32. Fraylick J.E., Riese M.J., Vincent T.S., Barbieri J.T., Olson J.C. ADP-ribosylation and functional effects of Pseudomonas exoenzyme S on cellular RalA. Biochemistry 2002, 41:9680-9687.
33. Zhang Y., Deng Q., Barbieri J.T. Intracellular localization of type III-delivered Pseudomonas ExoS with endosome vesicles. J. Biol. Chem. 2007, 282:13022-13032.
34. Goehring U.M., Schmidt G., Pederson K.J., Aktories K., Barbieri J.T. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem. 1999, 274:36369-36372.
35. Sun J., Maresso A.W., Kim J.J., Barbieri J.T. How bacterial ADP-ribosylating toxins recognize substrates. Nat. Struct. Mol. Biol. 2004, 11:868-876.
36. Krall R., Sun J., Pederson K.J., Barbieri J.T. In vivo rho GTPase-activating protein activity of Pseudomonas aeruginosa cytotoxin ExoS. Infect. Immun. 2002, 70:360-367.
37. Riese M.J., Barbieri J.T. Membrane localization contributes to the in vivo ADP-ribosylation of Ras by Pseudomonas aeruginosa ExoS. Infect. Immun. 2002, 70:2230-2232.
38. Zhang Y., Deng Q., Porath J.A., Williams C.L., Pederson-Gulrud K.J., Barbieri J.T. Plasma membrane localization affects the RhoGAP specificity of Pseudomonas ExoS. Cell. Microbiol. 2007, 9:2192-2201.
39. Vallis A.J., Yahr T.L., Barbieri J.T., Frank D.W. Regulation of ExoS production and secretion by Pseudomonas aeruginosa in response to tissue culture conditions. Infect. Immun. 1999, 67:914-920.
40. Knight D.A., Barbieri J.T. Ecto-ADP-ribosyltransferase activity of Pseudomonas aeruginosa exoenzyme S. Infect. Immun. 1997, 65:3304-3309.
41. Deng Q., Barbieri J.T. Modulation of host cell endocytosis by the type III cytotoxin, Pseudomonas ExoS. Traffic 2008, 9:1948-1957.
42. Radke J., Pederson K.J., Barbieri J.T. Pseudomonas aeruginosa exoenzyme S is a biglutamic acid ADP-ribosyltransferase. Infect. Immun. 1999, 67:1508-1510.