Activation of a bacterial virulence protein by the GTPase RhoA

Science Signaling

Volumn 2, Issue 95, 2009, Pages

  Christen, Matthias ^a   Coye, Lisette H ^a   Hontz, Jill S ^a   LaRock, Doris L ^a   Pfuetzner, Richard A ^a   Megha, ^a   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SSEJ PROTEIN; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; CHOLESTEROL;

ARTICLE; BACTERIAL VIRULENCE; CELL MEMBRANE; CELL VACUOLE; CHOLESTEROL ESTERIFICATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SALMONELLA CONTAINING VACUOLE; SALMONELLA TYPHIMURIUM; ESTERIFICATION; METABOLISM; SALMONELLA; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA;

BACTERIAL PROTEINS; CHOLESTEROL; ESTERIFICATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPASE; PROTEIN BINDING; RHOA GTP-BINDING PROTEIN; SALMONELLA; SIGNAL TRANSDUCTION; VIRULENCE FACTORS;

EID: 73949144553     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000430     Document Type: Article

References (25)

1. O. Steele-Mortimer, The Salmonella-containing vacuole: Moving with the times. Curr. Opin. Microbiol. 11, 38-45 (2008).
2. A. Haraga, M. B. Ohlson, S. I. Miller, Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6, 53-66 (2008).
3. M. Hensel, J. E. Shea, S. R. Waterman, R. Mundy, T. Nikolaus, G. Banks, A. Vazquez- Torres, C. Gleeson, F. C. Fang, D. W. Holden, Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30, 163-174 (1998).
4. D. Zhou, J. Galán, Salmonella entry into host cells: The work in concert of type III secreted effector proteins. Microbes Infect. 3, 1293-1298 (2001).
5. T. D. Lawley, K. Chan, L. J. Thompson, C. C. Kim, G. R. Govoni, D. M. Monack, Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2, e11 (2006).
6. J. Ruiz-Albert, X. J. Yu, C. R. Beuzón, A. N. Blakey, E. E. Galyov, D. W. Holden, Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol. Microbiol. 44, 645-661 (2002).
7. M. B. Ohlson, K. Fluhr, C. L. Birmingham, J. H. Brumell, S. I. Miller, SseJ deacylase activity by Salmonella enterica serovar Typhimurium promotes virulence in mice. Infect. Immun. 73, 6249-6259 (2005).
8. J. A. Freeman, M. E. Ohl, S. I. Miller, The Salmonella enterica serovar Typhimurium translocated effectors SseJ and SifB are targeted to the Salmonella-containing vacuole. Infect. Immun. 71, 418-427 (2003).
9. P. Nawabi, D. M. Catron, K. Haldar, Esterification of cholesterol by a type III secretion effector during intracellular Salmonella infection. Mol. Microbiol. 68, 173-185 (2008).
10. N. S. Lossi, N. Rolhion, A. I. Magee, C. Boyle, D. W. Holden, The Salmonella SPI-2 effector SseJ exhibits eukaryotic activator-dependent phospholipase A and glycerophospholipid: Cholesterol acyltransferase activity. Microbiology (Reading, England) 154, 2680-2688 (2008).
11. M. B. Ohlson, Z. Huang, N. M. Alto, M. P. Blanc, J. E. Dixon, J. Chai, S. I. Miller, Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA induce endosomal tubulation. Cell Host Microbe 4, 434-446 (2008).
12. S. J. Heasman, A. J. Ridley, Mammalian Rho GTPases: New insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701 (2008).
13. S. Etienne-Manneville, A. Hall, Rho GTPases in cell biology. Nature 420, 629-635 (2002).
14. K. Aktories, J. T. Barbieri, Bacterial cytotoxins: Targeting eukaryotic switches. Nat. Rev. Microbiol. 3, 397-410 (2005).
15. Y. Fu, J. E. Galán, A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297 (1999).
16. W. D. Hardt, L. M. Chen, K. E. Schuebel, X. R. Bustelo, J. E. Galán, S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826 (1998).
17. M. L. Yarbrough, Y. Li, L. N. Kinch, N. V. Grishin, H. L. Ball, K. Orth, AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323, 269-272 (2009).
18. G. Flatau, E. Lemichez, M. Gauthier, P. Chardin, S. Paris, C. Fiorentini, P. Boquet, Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387, 729-733 (1997).
19. S. C. Tsai, M. Noda, R. Adamik, J. Moss, M. Vaughan, Enhancement of choleragen ADP-ribosyltransferase activities by guanyl nucleotides and a 19-kDa membrane protein. Proc. Natl. Acad. Sci. U.S.A. 84, 5139-5142 (1987).
20. G. Schmidt, P. Sehr, M. Wilm, J. Selzer, M. Mann, K. Aktories, Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387, 725-729 (1997).
21. I. Just, J. Selzer, M. Wilm, C. von Eichel-Streiber, M. Mann, K. Aktories, Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375, 500-503 (1995).
22. D. M. Catron, M. D. Sylvester, Y. Lange, M. Kadekoppala, B. D. Jones, D. M. Monack, S. Falkow, K. Haldar, The Salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell. Microbiol. 4, 315-328 (2002).
23. S. E. Witowski, K. A. Walker, V. L. Miller, YspM, a newly identified Ysa type III secreted protein of Yersinia enterocolitica. J. Bacteriol. 190, 7315-7325 (2008).
24. E. Ikonen, Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138 (2008).
25. Acknowledgments: We thank D. A. Doyle from the Structural Genomics Consortium at the University of Oxford for the gift of the RhoB expression plasmid. We also thank L. Hoffman, H. Kulasekara, I. Levin, B. Kulasekara, and the Miller laboratory for discussions and critical reading of the manuscript. M.C. is supported by grants PBBSA-120489 and PA00P3-124140 from the Novartis Foundation and Swiss National Foundation. D.L. is supported by U.S. Public Health Service National Research Service Award T32 GM07270 from the National Institute of General Medical Sciences and S.I.M is supported by the NIH-National Institute of Allergy and Infectious Diseases grants R01 AI048683 and U54AI057141 for the Northwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases Research. Author contributions: S.I.M. supervised the project. M.C., L.H.C., J.S.H., D.L.L., R.A.P., and S.I.M. conducted the experiments in this study with the exception of the infection assays and microscopy, which were conducted by L.H.C. and M.C. M.C, L.H.C., and S.I.M. contributed to the writing of the manuscript.