Unraveling the mechanism of action of a new type III secretion system effector AexU from Aeromonas hydrophila

Microbial Pathogenesis

Volumn 49, Issue 3, 2010, Pages 122-134

  Sierra, Johanna C ^a   Suarez, Giovanni ^a   Sha, Jian ^a   Baze, Wallace B ^b   Foltz, Sheri M ^a   Chopra, Ashok K ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

ADP ribosyltransferase activity; Aeromonas hydrophila; AexU; Apoptosis; GAP activity; HeLa Tet Off cells; Septicemic mouse model of infection; Site directed mutagenesis; T3SS

Indexed keywords

BACTERIAL PROTEIN; CHEMOKINE; CYTOKINE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; I KAPPA B ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN AEXU; PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACTIN FILAMENT; AEROMONAS HYDROPHILA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL STRAIN; BACTERIUM DETECTION; CELL DISRUPTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MODIFICATION; GENE MUTATION; HELA CELL; HOST CELL; HUMAN; HUMAN CELL; LIVER; LUNG; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SPLEEN; SURVIVAL RATE; ANIMAL; ENZYMOLOGY; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; GRAM NEGATIVE INFECTION; HELA CELL LINE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; SECRETION (PROCESS); SURVIVAL;

AEROMONAS HYDROPHILA; ANIMALIA; MUS;

ADP RIBOSE TRANSFERASES; AEROMONAS HYDROPHILA; ANIMALS; BACTERIAL PROTEINS; CYTOKINES; GENE DELETION; GENETIC COMPLEMENTATION TEST; GRAM-NEGATIVE BACTERIAL INFECTIONS; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; LIVER; LUNG; MICE; SPLEEN; SURVIVAL ANALYSIS; VIRULENCE FACTORS;

EID: 77954648181     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2010.05.011     Document Type: Article

References (57)

1. Kuhn I., Albert M.J., Ansaruzzaman M., Bhuiyan N.A., Alabi S.A., Islam M.S., et al. Characterization of Aeromonas spp. isolated from humans with diarrhea, from healthy controls, and from surface water in Bangladesh. J Clin Microbiol 1997, 35:369-373.
2. Janda J.M., Guthertz L.S., Kokka R.P., Shimada T. Aeromonas species in septicemia: laboratory characteristics and clinical observations. Clin Infect Dis 1994, 19:77-83.
3. Brouqui P., Raoult D. Endocarditis due to rare and fastidious bacteria. Clin Microbiol Rev 2001, 14:177-207.
4. Palu A.P., Gomes L.M., Miguel M.A., Balassiano I.T., Queiroz M.L., Freitas-Almeida A.C., et al. Antimicrobial resistance in food and clinical Aeromonas isolates. Food Microbiol 2006, 23:504-509.
5. Altwegg M., Martinetti Lucchini G., Luthy-Hottenstein J., Rohrbach M. Aeromonas-associated gastroenteritis after consumption of contaminated shrimp. Eur J Clin Microbiol Infect Dis 1991, 10:44-45.
6. Kirov S.M. The public health significance of Aeromonas spp. in foods. Int J Food Microbiol 1993, 20:179-198.
7. Edberg S.C., Browne F.A., Allen M.J. Issues for microbial regulation: Aeromonas as a model. Crit Rev Microbiol 2007, 33:89-100.
8. Chopra A.K., Houston C.W. Enterotoxins in Aeromonas-associated gastroenteritis. Microbes Infect 1999, 1:1129-1137.
9. Chopra A.K., Xu X., Ribardo D., Gonzalez M., Kuhl K., Peterson J.W., et al. The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Infect Immun 2000, 68:2808-2818.
10. Ferguson M.R., Xu X.J., Houston C.W., Peterson J.W., Coppenhaver D.H., Popov V.L., et al. Hyperproduction, purification, and mechanism of action of the cytotoxic enterotoxin produced by Aeromonas hydrophila. Infect Immun 1997, 65:4299-4308.
11. Galindo C.L., Sha J., Fadl A.A., Pillai L., Chopra A.K. Host immune responses to Aeromonas virulence factors. Curr Immunol Rev 2006, 2:13-26.
12. Ribardo D.A., Kuhl K.R., Boldogh I., Peterson J.W., Houston C.W., Chopra A.K. Early cell signaling by the cytotoxic enterotoxin of Aeromonas hydrophila in macrophages. Microb Pathog 2002, 32:149-163.
13. Galindo C.L., Fadl A.A., Sha J., Gutierrez C., Popov V.L., Boldogh I., et al. Aeromonas hydrophila cytotoxic enterotoxin activates mitogen-activated protein kinases and induces apoptosis in murine macrophages and human intestinal epithelial cells. J Biol Chem 2004, 279:37597-37612.
14. Sierra J.C., Suarez G., Sha J., Foltz S.M., Popov V.L., Galindo C.L., et al. Biological characterization of a new type III secretion system effector from a clinical isolate of Aeromonas hydrophila-part II. Microb Pathog 2007, 43:147-160.
15. Sha J., Wang S.F., Suarez G., Sierra J.C., Fadl A.A., Erova T.E., et al. Further characterization of a type III secretion system (T3SS) and of a new effector protein from a clinical isolate of Aeromonas hydrophila-part I. Microb Pathog 2007, 43:127-146.
16. Braun M., Stuber K., Schlatter Y., Wahli T., Kuhnert P., Frey J. Characterization of an ADP-ribosyltransferase toxin (AexT) from Aeromonas salmonicida subsp. salmonicida. J Bacteriol 2002, 184:1851-1858.
17. Fehr D., Burr S.E., Gibert M., d'Alayer J., Frey J., Popoff M.R. Aeromonas exoenzyme T of Aeromonas salmonicida is a bifunctional protein that targets the host cytoskeleton. J Biol Chem 2007, 282:28843-28852.
18. Henriksson M.L., Sundin C., Jansson A.L., Forsberg A., Palmer R.H., Hallberg B. Exoenzyme S shows selective ADP-ribosylation and GTPase-activating protein (GAP) activities towards small GTPases in vivo. Biochem J 2002, 367:617-628.
19. Barbieri J.T., Sun J. Pseudomonas aeruginosa ExoS and ExoT. Rev Physiol Biochem Pharmacol 2004, 152:79-92.
20. Krall R., Schmidt G., Aktories K., Barbieri J.T. Pseudomonas aeruginosa ExoT is a Rho GTPase-activating protein. Infect Immun 2000, 68:6066-6068.
21. Burr S.E., Stuber K., Frey J. The ADP-ribosylating toxin, AexT, from Aeromonas salmonicida subsp. salmonicida is translocated via a type III secretion pathway. J Bacteriol 2003, 185:6583-6591.
22. Zhang Y., Barbieri J.T. A leucine-rich motif targets Pseudomonas aeruginosa ExoS within mammalian cells. Infect Immun 2005, 73:7938-7945.
23. 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.
24. Aktories K., Barbieri J.T. Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 2005, 3:397-410.
25. Fiorentini C., Falzano L., Travaglione S., Fabbri A. Hijacking Rho GTPases by protein toxins and apoptosis: molecular strategies of pathogenic bacteria. Cell Death Differ 2003, 10:147-152.
26. Aktories K., Schmidt G., Just I. Rho GTPases as targets of bacterial protein toxins. Biol Chem 2000, 381:421-426.
27. Scheffzek K., Ahmadian M.R., Wittinghofer A. GTPase-activating proteins: helping hands to complement an active site. Trends Biochem Sci 1998, 23:257-262.
28. Montaner S., Perona R., Saniger L., Lacal J.C. Multiple signalling pathways lead to the activation of the nuclear factor kappaB by the Rho family of GTPases. J Biol Chem 1998, 273:12779-12785.
29. Perona R., Montaner S., Saniger L., Sanchez-Perez I., Bravo R., Lacal J.C. Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins. Genes Dev 1997, 11:463-475.
30. Coso O.A., Chiariello M., Yu J.C., Teramoto H., Crespo P., Xu N., et al. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995, 81:1137-1146.
31. Minden A., Lin A., Claret F.X., Abo A., Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995, 81:1147-1157.
32. Naumann M. Nuclear factor-kappa B activation and innate immune response in microbial pathogen infection. Biochem Pharmacol 2000, 60:1109-1114.
33. Hedges S.R., Agace W.W., Svanborg C. Epithelial cytokine responses and mucosal cytokine networks. Trends Microbiol 1995, 3:266-270.
34. Xu X.J., Ferguson M.R., Popov V.L., Houston C.W., Peterson J.W., Chopra A.K. Role of a cytotoxic enterotoxin in Aeromonas-mediated infections: development of transposon and isogenic mutants. Infect Immun 1998, 66:3501-3509.
35. Holbourn K.P., Shone C.C., Acharya K.R. A family of killer toxins. Exploring the mechanism of ADP-ribosylating toxins. FEBS J 2006, 273:4579-4593.
36. Han S., Tainer J.A. The ARTT motif and a unified structural understanding of substrate recognition in ADP-ribosylating bacterial toxins and eukaryotic ADP-ribosyltransferases. Int J Med Microbiol 2002, 291:523-529.
37. Liu S., Kulich S.M., Barbieri J.T. Identification of glutamic acid 381 as a candidate active site residue of Pseudomonas aeruginosa exoenzyme S. Biochemistry 1996, 35:2754-2758.
38. Suarez G., Sierra J.C., Erova T.E., Sha J., Horneman A.J., Chopra A.K. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol 2010, 192:155-168.
39. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005, 21:247-269.
40. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
41. Hall A. Rho GTPases and the control of cell behaviour. Biochem Soc Trans 2005, 33:891-895.
42. Kaufman M.R., Jia J., Zeng L., Ha U., Chow M., Jin S. Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of exoS. Microbiology 2000, 146(Pt 10):2531-2541.
43. Galle M., Schotte P., Haegman M., Wullaert A., Yang H.J., Jin S., et al. The Pseudomonas aeruginosa Type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1beta maturation. J Cell Mol Med 2008, 12:1767-1776.
44. Hippenstiel S., Schmeck B., N'Guessan P.D., Seybold J., Krull M., Preissner K., et al. Rho protein inactivation induced apoptosis of cultured human endothelial cells. Am J Physiol Lung Cell Mol Physiol 2002, 283:L830-L838.
45. Blanco-Colio L.M., Villa A., Ortego M., Hernandez-Presa M.A., Pascual A., Plaza J.J., et al. 3-Hydroxy-3-methyl-glutaryl coenzyme A reductase inhibitors, atorvastatin and simvastatin, induce apoptosis of vascular smooth muscle cells by downregulation of Bcl-2 expression and Rho A prenylation. Atherosclerosis 2002, 161:17-26.
46. Bobak D.A. Clostridial toxins: molecular probes of Rho-dependent signaling and apoptosis. Mol Cell Biochem 1999, 193:37-42.
47. Moorman J.P., Bobak D.A., Hahn C.S. Inactivation of the small GTP binding protein Rho induces multinucleate cell formation and apoptosis in murine T lymphoma EL4. J Immunol 1996, 156:4146-4153.
48. Tato C.M., Hunter C.A. Host-pathogen interactions: subversion and utilization of the NF-kappa B pathway during infection. Infect Immun 2002, 70:3311-3317.
49. Sha J., Kozlova E.V., Fadl A.A., Olano J.P., Houston C.W., Peterson J.W., et al. Molecular characterization of a glucose-inhibited division gene, gidA, that regulates cytotoxic enterotoxin of Aeromonas hydrophila. Infect Immun 2004, 72:1084-1095.
50. Sha J., Erova T.E., Alyea R.A., Wang S., Olano J.P., Pancholi V., et al. Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J Bacteriol 2009, 191:3095-3107.
51. Esch T., Stefano G. Proinflammation: a common denominator or initiator of different pathophysiological disease processes. Med Sci Monit 2002, 8:HY1-HY9.
52. Lee S.C., Brummet M.E., Shahabuddin S., Woodworth T.G., Georas S.N., Leiferman K.M., et al. Cutaneous injection of human subjects with macrophage inflammatory protein-1 alpha induces significant recruitment of neutrophils and monocytes. J Immunol 2000, 164:3392-3401.
53. Cavaillon J.M., Adib-Conquy M., Fitting C., Adrie C., Payen D. Cytokine cascade in sepsis. Scand J Infect Dis 2003, 35:535-544.
54. Osuchowski M.F., Welch K., Siddiqui J., Remick D.G. Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J Immunol 2006, 177:1967-1974.
55. Cohen J. The immunopathogenesis of sepsis. Nature 2002, 420:885-891.
56. Bergsbaken T., Fink S.L., Cookson B.T. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009, 7:99-109.
57. Coligan Current protocols in protein science 2002, vol. 2. John Wiley & Sons, Inc., New York.