Recombinant AexU effector protein of Aeromonas veronii bv. sobria disrupts the actin cytoskeleton by downregulation of Rac1 and induces direct cytotoxicity to β4-integrin expressing cell lines

Microbial Pathogenesis

Volumn 51, Issue 6, 2011, Pages 454-465

  Abolghait, Said Kamal ^a,c   Iida, Tetsuya ^b   Kodama, Toshio ^a   Cantarelli, Vlademir V ^a,d   Akeda, Yukihiro ^a   Honda, Takeshi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c Suez Canal University   (Egypt)

^d UNIVERSIDADE FEEVALE   (Brazil)

Author keywords

4 Integrin; Aeromonas; AexU; Cytotoxicity; Rac1

Indexed keywords

ACTIN; AEXU PROTEIN; ALANINE; ARGININE; ASPARAGINE; BACTERIAL PROTEIN; BETA4 INTEGRIN; GLYCINE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTEGRIN; PROTEIN CDC42; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

AEROMONAS VERONII; AEXU GENE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DISRUPTION; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; DOWN REGULATION; ENZYME INACTIVATION; GENE EXPRESSION REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SUBSPECIES; TRANSIENT TRANSFECTION; TYPE III SECRETION SYSTEM;

ACTIN CYTOSKELETON; AEROMONAS; AMINO ACID SUBSTITUTION; ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL SURVIVAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INTEGRIN BETA4; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RAC1 GTP-BINDING PROTEIN; RECOMBINANT PROTEINS; VIRULENCE FACTORS;

AEROMONAS; AEROMONAS HYDROPHILA; AEROMONAS VERONII BV. SOBRIA;

EID: 80054836990     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2011.09.006     Document Type: Article

References (41)

1. Shiina Y., Ii K., Iwanaga M. An Aeromonas veronii biovar sobria infection with disseminated intravascular gas production. J Infect Chemother 2004, 10:37-41.
2. Song T., Toma C., Nakasone N., Iwanaga M. Aerolysin is activated by metalloprotease in Aeromonas veronii biovar sobria. J Med Microbiol 2004, 53:477-482.
3. Ghosh P. Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 2004, 68:771-795.
4. 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.
5. Litvak Y., Selinger Z. Aeromonas salmonicida toxin AexT has a Rho family GTPase-activating protein domain. J Bacteriol 2007, 189:2558-2560.
6. 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.
7. Vilches S., Wilhelms M., Yu H.B., Leung K.Y., Tomas J.M., Merino S. Aeromonas hydrophila AH-3 AexT is an ADP-ribosylating toxin secreted through the type III secretion system. Microb Pathog 2008, 44:1-12.
8. Chacon M.R., Soler L., Groisman E.A., Guarro J., Figueras M.J. Type III secretion system genes in clinical Aeromonas isolates. J Clin Microbiol 2004, 42:1285-1287.
9. 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.
10. 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.
11. Silver A.C., Graf J. Prevalence of genes encoding the type three secretion system and the effectors AexT and AexU in the Aeromonas veronii group. DNA Cell Biol 2009, 28:383-388.
12. Sierra J.C., Suarez G., Sha J., Baze W.B., Foltz S.M., Chopra A.K. Unraveling the mechanism of action of a new type III secretion system effector AexU from Aeromonas hydrophila. Microb Pathog 2010, 49:122-134.
13. Balasubramanian S., Kuppuswamy D. RGD-containing peptides activate S6K1 through beta3 integrin in adult cardiac muscle cells. J Biol Chem 2003, 278:42214-42224.
14. Ballarin L., Burighel P. RGD-containing molecules induce macropinocytosis in ascidian hyaline amoebocytes. J Invertebr Pathol 2006, 91:124-130.
15. Chang A.C., Cohen S.N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 1978, 134:1141-1156.
16. Akeda Y., Kodama T., Kashimoto T., Cantarelli V., Horiguchi Y., Nagayama K., et al. Dominant-negative Rho, Rac, and Cdc42 facilitate the invasion process of Vibrio parahaemolyticus into Caco-2 cells. Infect Immun 2002, 70:970-973.
17. Cantarelli V.V., Kodama T., Nijstad N., Abolghait S.K., Iida T., Honda T. Cortactin is essential for F-actin assembly in enteropathogenic Escherichia coli (EPEC)- and enterohaemorrhagic E. coli (EHEC)-induced pedestals and the alpha-helical region is involved in the localization of cortactin to bacterial attachment sites. Cell Microbiol 2006, 8:769-780.
18. Fengqing H., Song Y. Electroporation-mediated transformation of Aeromonas hydrophila. Plasmid 2005, 54:283-287.
19. 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.
20. Mateu M.G., Valero M.L., Andreu D., Domingo E. Systematic replacement of amino acid residues within an Arg-Gly-Asp-containing loop of foot-and-mouth disease virus and effect on cell recognition. J Biol Chem 1996, 271:12814-12819.
21. Hausner S.H., Dicara D., Marik J., Marshall J.F., Sutcliffe J.L. Use of a peptide derived from foot-and-mouth disease virus for the noninvasive imaging of human cancer: generation and evaluation of 4-[18F]fluorobenzoyl A20FMDV2 for in vivo imaging of integrin {alpha}v{beta}6 expression with positron emission tomography. Cancer Res 2007, 67:7833-7840.
22. 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.
23. Simon-Assmann P., Leberquier C., Molto N., Uezato T., Bouziges F., Kedinger M. Adhesive properties and integrin expression profiles of two colonic cancer populations differing by their spreading on laminin. J Cell Sci 1994, 107(Pt 3):577-587.
24. Tcherkezian J., Lamarche-Vane N. Current knowledge of the large RhoGAP family of proteins. Biol Cell 2007, 99:67-86.
25. Boquet P., Lemichez E. Bacterial virulence factors targeting Rho GTPases: parasitism or symbiosis?. Trends Cell Biol 2003, 13:238-246.
26. 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.
27. Von Pawel-Rammingen U., Telepnev M.V., Schmidt G., Aktories K., Wolf-Watz H., Rosqvist R. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol Microbiol 2000, 36:737-748.
28. Wurtele M., Wolf E., Pederson K.J., Buchwald G., Ahmadian M.R., Barbieri J.T., et al. How the Pseudomonas aeruginosa ExoS toxin downregulates Rac. Nat Struct Biol 2001, 8:23-26.
29. Burr S.E., Stuber K., Wahli T., Frey J. Evidence for a type III secretion system in Aeromonas salmonicida subsp. salmonicida. J Bacteriol 2002, 184:5966-5970.
30. 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.
31. Mohri T., Adachi Y., Ikehara S., Hioki K., Tokunaga R., Taketani S. Activated Rac1 selectively up-regulates the expression of integrin alpha6beta4 and induces cell adhesion and membrane ruffles of nonadherent colon cancer Colo201 cells. Exp Cell Res 1999, 253:533-540.
32. Pullar C.E., Baier B.S., Kariya Y., Russell A.J., Horst B.A., Marinkovich M.P., et al. beta4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1. Mol Biol Cell 2006, 17:4925-4935.
33. West M.A., Prescott A.R., Eskelinen E.L., Ridley A.J., Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 2000, 10:839-848.
34. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
35. Lee E.C., Lotz M.M., Steele G.D., Mercurio A.M. The integrin alpha 6 beta 4 is a laminin receptor. J Cell Biol 1992, 117:671-678.
36. Stepp M.A., Spurr-Michaud S., Tisdale A., Elwell J., Gipson I.K. Alpha 6 beta 4 integrin heterodimer is a component of hemidesmosomes. Proc Natl Acad Sci U S A 1990, 87:8970-8974.
37. Rabinovitz I., Mercurio A.M. The integrin alpha 6 beta 4 and the biology of carcinoma. Biochem Cell Biol 1996, 74:811-821.
38. Cruz-Monserrate Z., Qiu S., Evers B.M., O'Connor K.L. Upregulation and redistribution of integrin alpha6beta4 expression occurs at an early stage in pancreatic adenocarcinoma progression. Mod Pathol 2007, 20:656-667.
39. Giannelli G., Astigiano S., Antonaci S., Morini M., Barbieri O., Noonan D.M., et al. Role of the alpha3beta1 and alpha6beta4 integrins in tumor invasion. Clin Exp Metastasis 2002, 19:217-223.
40. Beaulieu J.F. Integrins and human intestinal cell functions. Front Biosci 1999, 4:D310-D321.
41. Kumano M., Miyake H., Honda T., Fujisawa M. Characterization of beta4-integrin-mediated cytotoxic effect of AexU, a type three secretion system effector, on human prostate cancer pc3 cells. J Urol 2010, 183:e151-e152.