The ADP-ribosylation domain of Pseudomonas aeruginosa ExoS is required for membrane bleb niche formation and bacterial survival within epithelial cells

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4500-4510

  Angus, Annette A ^a,f   Evans, David J ^b,d   Barbieri, Joseph T ^e   Fleiszig, Suzanne M J ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TOURO UNIVERSITY CALIFORNIA   (United States)

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; LIPOCORTIN 5; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RAB PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; APOPTOSIS; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CELL DIVISION; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PSEUDOMONAS AERUGINOSA; WILD TYPE;

ADP RIBOSE TRANSFERASES; BACTERIAL TOXINS; CELL LINE; CELL MEMBRANE; CELLULAR STRUCTURES; CORNEA; ECOSYSTEM; EPITHELIAL CELLS; HUMANS; MICROBIAL VIABILITY; PSEUDOMONAS AERUGINOSA;

EID: 78049431931     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00417-10     Document Type: Article

References (58)

1. Angus, A. A., A. A. Lee, D. K. Augustin, E. J. Lee, D. J. Evans, and S. M. Fleiszig. 2008. Pseudomonas aeruginosa induces membrane blebs in epithelial cells, which are utilized as a niche for intracellular replication and motility. Infect. Immun. 76:1992-2001.
2. Barbieri, J. T. 2000. Pseudomonas aeruginosa exoenzyme S, a bifunctional type-III secreted cytotoxin. Int. J. Med. Microbiol. 290:381-387.
3. Barbieri, J. T., and J. Sun. 2004. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol. 152:79-92.
4. Charras, G., and E. Paluch. 2008. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 9:730-736.
5. Charras, G. T. 2008. A short history of blebbing. J. Microsc. 231:466-478.
6. Cossart, P., and P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242-248.
7. Cowell, B. A., D. Y. Chen, D. W. Frank, A. J. Vallis, and S. M. Fleiszig. 2000. ExoT of cytotoxic Pseudomonas aeruginosa prevents uptake by corneal epithelial cells. Infect. Immun. 68:403-406.
8. Cowell, B. A., D. J. Evans, and S. M. Fleiszig. 2005. Actin cytoskeleton disruption by ExoY and its effects on Pseudomonas aeruginosa invasion. FEMS Microbiol. Lett. 250:71-76.
9. Deng, Q., and J. T. Barbieri. 2008. Modulation of host cell endocytosis by the type III cytotoxin, Pseudomonas ExoS. Traffic 9:1948-1957.
10. Engel, J., and P. Balachandran. 2009. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 12:61-66.
11. Evans, D., T. Kuo, M. Kwong, R. Van, and S. Fleiszig. 2002. Pseudomonas aeruginosa strains with lipopolysaccharide defects exhibit reduced intracellular viability after invasion of corneal epithelial cells. Exp. Eye Res. 75:635-643.
12. Evans, D. J., D. W. Frank, V. Finck-Barbancon, C. Wu, and S. M. Fleiszig. 1998. Pseudomonas aeruginosa invasion and cytotoxicity are independent events, both of which involve protein tyrosine kinase activity. Infect. Immun. 66:1453-1459.
13. Fackler, O. T., and R. Grosse. 2008. Cell motility through plasma membrane blebbing. J. Cell Biol. 181:879-884.
14. 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.
15. Finck-Barbançon, V., J. Goranson, L. Zhu, T. Sawa, J. P. Wiener-Kronish, S. M. Fleiszig, C. Wu, L. Mende-Mueller, and D. W. Frank. 1997. ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol. Microbiol. 25:547-557.
16. Fleiszig, S. M., J. P. Wiener-Kronish, H. Miyazaki, V. Vallas, K. E. Mostov, D. Kanada, T. Sawa, T. S. Yen, and D. W. Frank. 1997. Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 65:579-586.
17. Fleiszig, S. M., T. S. Zaidi, E. L. Fletcher, M. J. Preston, and G. B. Pier. 1994. Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect. Immun. 62:3485-3493.
18. Fleiszig, S. M., T. S. Zaidi, and G. B. Pier. 1995. Pseudomonas aeruginosa invasion of and multiplication within corneal epithelial cells in vitro. Infect. Immun. 63:4072-4077.
19. 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.
20. Ganesan, A. K., D. W. Frank, R. P. Misra, G. Schmidt, and J. T. Barbieri. 1998. Pseudomonas aeruginosa exoenzyme S ADP-ribosylates Ras at multiple sites. J. Biol. Chem. 273:7332-7337.
21. Garrity-Ryan, L., B. Kazmierczak, R. Kowal, J. Comolli, A. Hauser, and J. N. Engel. 2000. The arginine finger domain of ExoT contributes to actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect. Immun. 68:7100-7113.
22. Garrity-Ryan, L., S. Shafikhani, P. Balachandran, L. Nguyen, J. Oza, T. Jakobsen, J. Sargent, X. Fang, S. Cordwell, M. A. Matthay, and J. N. Engel. 2004. The ADP ribosyltransferase domain of Pseudomonas aeruginosa ExoT contributes to its biological activities. Infect. Immun. 72:546-558.
23. Gooderham, W. J., and R. E. Hancock. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 33:279-294.
24. Hauser, A. R. 2009. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat. Rev. Microbiol. 7:654-665.
25. Hauser, A. R., and J. N. Engel. 1999. Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect. Immun. 67:5530-5537.
26. Hauser, A. R., S. Fleiszig, P. J. Kang, K. Mostov, and J. N. Engel. 1998. Defects in type III secretion correlate with internalization of Pseudomonas aeruginosa by epithelial cells. Infect. Immun. 66:1413-1420.
27. Hazlett, L. D. 2007. Bacterial infections of the cornea (Pseudomonas aeruginosa). Chem. Immunol. Allergy 92:185-194.
28. Herman, B., G. J. Gores, A. L. Nieminen, T. Kawanishi, A. Harman, and J. J. Lemasters. 1990. Calcium and pH in anoxic and toxic injury. Crit. Rev. Toxicol. 21:127-148.
29. Jia, J., Y. Wang, L. Zhou, and S. Jin. 2006. Expression of Pseudomonas aeruginosa toxin ExoS effectively induces apoptosis in host cells. Infect. Immun. 74:6557-6570.
30. Kaufman, M. R., J. Jia, L. Zeng, U. Ha, M. Chow, and S. Jin. 2000. Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of exoS. Microbiology 146:2531-2541.
31. Lee, E. J., B. A. Cowell, D. J. Evans, and S. M. Fleiszig. 2003. Contribution of ExsA-regulated factors to corneal infection by cytotoxic and invasive Pseudomonas aeruginosa in a murine scarification model. Invest. Ophthalmol. Vis. Sci. 44:3892-3898.
32. Lee, V. T., R. S. Smith, B. Tummler, and S. Lory. 2005. Activities of Pseudomonas aeruginosa effectors secreted by the type III secretion system in vitro and during infection. Infect. Immun. 73:1695-1705.
33. Liu, S., S. M. Kulich, and J. T. Barbieri. 1996. Identification of glutamic acid 381 as a candidate active site residue of Pseudomonas aeruginosa exoenzyme S. Biochemistry 35:2754-2758.
34. Liu, S., T. L. Yahr, D. W. Frank, and J. T. Barbieri. 1997. Biochemical relationships between the 53-kilodalton (Exo53) and 49-kilodalton (ExoS) forms of exoenzyme S of Pseudomonas aeruginosa. J. Bacteriol. 179:1609-1613.
35. 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.
36. Maresso, A. W., Q. Deng, M. S. Pereckas, B. T. Wakim, and J. T. Barbieri. 2007. Pseudomonas aeruginosa ExoS ADP-ribosyltransferase inhibits ERM phosphorylation. Cell. Microbiol. 9:97-105.
37. Marin-Castaño, M. E., K. G. Csaky, and S. W. Cousins. 2005. Nonlethal oxidant injury to human retinal pigment epithelium cells causes cell membrane blebbing but decreased MMP-2 activity. Invest. Ophthalmol. Vis. Sci. 46:3331-3340.
38. Masters, S. C., K. J. Pederson, L. Zhang, J. T. Barbieri, and H. Fu. 1999. Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. Biochemistry 38:5216-5221.
39. Olson, J. C., J. E. Fraylick, E. M. McGuffie, K. M. Dolan, T. L. Yahr, D. W. Frank, and T. S. Vincent. 1999. Interruption of multiple cellular processes in HT-29 epithelial cells by Pseudomonas aeruginosa exoenzyme S. Infect. Immun. 67:2847-2854.
40. Page, M. G., and J. Heim. 2009. Prospects for the next anti-Pseudomonas drug. Curr. Opin. Pharmacol. 9:558-565.
41. Pederson, K. J., R. Krall, M. J. Riese, and J. T. Barbieri. 2002. Intracellular localization modulates targeting of ExoS, a type III cytotoxin, to eukaryotic signalling proteins. Mol. Microbiol. 46:1381-1390.
42. Pederson, K. J., S. Pal, A. J. Vallis, D. W. Frank, and J. T. Barbieri. 2000. Intracellular localization and processing of Pseudomonas aeruginosa ExoS in eukaryotic cells. Mol. Microbiol. 37:287-299.
43. 2+- dependent, PKC-mediated mechanism: protective effect of PKA. Free Radic. Biol. Med. 40:2005-2017.
44. 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.
45. Robertson, D. M., L. Li, S. Fisher, V. P. Pearce, J. W. Shay, W. E. Wright, H. D. Cavanagh, and J. V. Jester. 2005. Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Invest. Ophthalmol. Vis Sci. 46:470-478.
46. Sen, S. 1992. Programmed cell death: concept, mechanism and control. Biol. Rev. Camb. Philos. Soc. 67:287-319.
47. Shaver, C. M., and A. R. Hauser. 2004. Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect. Immun. 72:6969-6977.
48. Soong, G., D. Parker, M. Magargee, and A. S. Prince. 2008. The type III toxins of Pseudomonas aeruginosa disrupt epithelial barrier function. J. Bacteriol. 190:2814-2821.
49. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
50. 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.
51. van Heerde, W. L., S. Robert-Offerman, E. Dumont, L. Hofstra, P. A. Doevendans, J. F. Smits, M. J. Daemen, and C. P. Reutelingsperger. 2000. Markers of apoptosis in cardiovascular tissues: focus on Annexin V. Cardiovasc. Res. 45:549-559.
52. Wagner, V. E., and B. H. Iglewski. 2008. P. aeruginosa biofilms in CF infection. Clin. Rev. Allergy Immunol. 35:124-134.
53. Willcox, M. D. 2007. Pseudomonas aeruginosa infection and inflammation during contact lens wear: a review. Optom. Vis. Sci. 84:273-278.
54. Yahr, T. L., and D. W. Frank. 1994. Transcriptional organization of the trans-regulatory locus which controls exoenzyme S synthesis in Pseudomonas aeruginosa. J. Bacteriol. 176:3832-3838.
55. 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. U. S. A. 95:13899-13904.
56. Yahr, T. L., and M. C. Wolfgang. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 62:631-640.
57. Zaidi, T. S., J. Lyczak, M. Preston, and G. B. Pier. 1999. Cystic fibrosis transmembrane conductance regulator-mediated corneal epithelial cell ingestion of Pseudomonas aeruginosa is a key component in the pathogenesis of experimental murine keratitis. Infect. Immun. 67:1481-1492.
58. Zhang, Y., Q. Deng, and J. T. Barbieri. 2007. Intracellular localization of type III-delivered Pseudomonas ExoS with endosome vesicles. J. Biol. Chem. 282:13022-13032.