GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: A mechanism for disruption of actin microfilament structure

Molecular Microbiology

Volumn 36, Issue 3, 2000, Pages 737-748

  Von Pawel Rammingen, Ulrich ^a,c   Telepnev, Maxim V ^a   Schmidt, Gudula ^b   Aktories, Klaus ^b   Wolf Watz, Hans ^a   Rosqvist, Roland ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF FREIBURG   (Germany)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ARGININE; BACTERIAL TOXIN; CELL CYCLE PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAC PROTEIN; RHO FACTOR;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; HELA CELL; HUMAN; HUMAN CELL; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; YERSINIA; YERSINIA PSEUDOTUBERCULOSIS;

ACTINS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; GTPASE-ACTIVATING PROTEINS; HELA CELLS; HUMANS; KINETICS; MICROFILAMENTS; RECOMBINANT PROTEINS; RHO GTP-BINDING PROTEINS; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SACCHAROMYCES CEREVISIAE; YERSINIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0034097414     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01898.x     Document Type: Article

References (37)

1. Agatep, R., Kirkpatrick, R.D., Parchaliuk, D.L., Woods, R.A., and Gietz, R.D. (1998) Transformation of Sacchammyces cerevisiae by the lithium acelate/single-stranded carrier DNA/polyethylene glycol (LiAc/ss-DNA/PEG) protocol. Technical Tips Online.
2. Aktories, K. (1997) Rho proteins: targets for bacterial toxins. Trends Microbiol 5: 282-287.
3. Aktories, K., and Koch, G. (1997) Clostridium botulinum ADP-ribosyltransferase C3. In Bacterial Toxins: Tools in Cell Biology and Pharmacology. Aktories, K. (ed. ). Weinheim: Chapman & Hall, pp. 61-69.
4. Bickle, M., Delley, P.A., Schmidt, A., and Hall, M.N. (1998) Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J 17: 2235-2245.
5. Black, D.S., and Bliska, J.B. (1997) Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J 16: 2730-2744.
6. Bliska, J.B., and Black, D.S. (1995) Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase. Infect Immun 63: 681-685.
7. Blumer, K.J., Johnson, G.L., and Lange-Carter, C.A. (1994) Mammalian mitogen-activated protein kinase kinase kinase (MEKK) can function in a yeast mitogen-activated protein kinase pathway downstream of protein kinase C. Proc Natl Acad Sci USA 91: 4925-4929.
8. Boland, A., Sory, M.P., Iriarte, M., Kerbourch, C., Wattiau, P., and Cornelis, G.R. (1996) Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus. EMBO J 15: 5191-5201.
9. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., and Hieter, P. (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
10. Cornelis, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
11. Cover, T.L., and Aber, R.C. (1989) Yersinia enterocolitica. N Engl J Med 321: 16-24.
12. Doyle, T., and Bostein, D. (1996) Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93: 3886-3891.
13. Drgonová, J., Drgon, T., Tanaka, K., Kollar, R., Chen, G.C., Ford, R.A., et al. (1996) Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272: 277-279.
14. Drgonová, J., Drgon, T., Roh, D.H., and Cabib, E. (1999) The GTP-binding protein Rho1p is required for cell cycle progression and polarization of the yeast cell. J Cell Biol 146: 373-387.
15. Evangelista, M., Blundell, K., Longtine, M.S., Chow, C.J., Adames, N., Pringle, J.R., et al. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118-122.
16. Fällman, M., Andersson, K., Håkansson, S., Magnusson, K.E., Stendahl, O., and Wolf-Watz, H. (1995) Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 63: 3117-3124.
17. Fiorentini, C., Fabbri, A., Flatau, G., Donelli, G., Matarrese, P., Lemichez, E., et al. (1997) Escherichia coli cytotoxic necrotizing factor 1 (CNF-1), a toxin that activates the Rho GTPase. J Biol Chem 272: 19532-19537.
18. Flatau, G., Lemichez, E., Gauthier, M., Chardin, P., Paris, S., Florentini, C., et al. (1997) Toxin induced activation of the G protein p21 Rho by dėamidation of glutamine. Nature 387: 729-733.
19. Forsberg, Ȧ., and Wolf-Watz, H. (1988) The virulence protein Yop5 of Yersinia pseudotuberculosis is regulated at transcriptional level by plasmid-plB1-encoded trans-acting elements controlled by temperature and calcium. Mol Microbiol 2: 121-133.
20. Frithz-Lindsten, E., Du, Y., Rosqvist, R., and Forsberg, A. (1997) Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol Microbiol 6: 1125-1139.
21. Fu, Y., and Galán, J.E. (1999) A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401: 293-297.
22. Goehring, U.-M., Schmidt, G., Pederson, K.J., Aktories, K., and Barbieri, J. (1999) The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase activating protein for Rho GTPases. J Biol Chem 274: 36369-36372.
23. Hȧkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homble, F., et al. (1996) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15: 5812-5823.
24. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
25. Heesemann, J., Algermissen, B., and Laufs, R. (1984) Genetically manipulated virulence of Yersinia enterocolitica. Infect Immun 46: 105-110.
26. Helliwell, S.B., Schmidt, A., Ohya, Y., and Hall, M.N. (1998) The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr Biol 8: 1211-1214.
27. Herskowitz, I. (1995) MAP kinase pathways in yeast: for mating and more. Cell 80: 187-197.
28. Imamura, H., Tanaka, K., Hihara, T., Umikawa, M., Kamei, T., Takahashi, K., et al. (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J 16: 2745-2755.
29. Jacoby, J.J., Nilius, S.M., and Heinisch, J.J. (1998) A screen for upstream components of the yeast protein kinase C signal transduction pathway identifies the product of the SLG1 gene. Mol Gen Genet 258: 148-155.
30. Just, I., Selzer, J., von Eichel-Streiber, C., Mann, M., and Aktories, K. (1995a) Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375: 500-503.
31. Just, I., Wilm, M., Selzer, J., Rex, G., von Eichel-Streiber, C., Mann, M., et al. (1995b) The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the Rho proteins. J Biol Chem 270: 13932-13936.
32. Just, I., Selzer, J., Hofmann, F., Green, G.A., and Aktories, K. (1996) Inactivation of Ras by Clostridium sordellii lethal toxin-catalyzed glucosylation. J Biol Chem 271: 10149-10153.
33. Kamada, Y., Qadota, H., Python, C.P., Anraku, Y., Ohya, Y., and Levin, D.E. (1996) Activation of yeast protein kinase C by Rho1 GTPase. J Biol Chem 271: 9193-9196.
34. Kohno, H., Tanaka, K., Mino, A., Umikawa, M., Imamura, H., Fujiwara, T., et al. (1996) Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J 15: 6060-6068.
35. Kozma, R., Ahmed, S., Best, A., and Lim, L. (1995) The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Bioll 15: 1942-1952.
36. Lee, K.S., and Levin, D.E. (1992) Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homologue. Mol Cell Biol 12: 172-182.
37. Lerm, M., Selzer, J., Hoffmeyer, A., Rapp, U.R., Aktories, K., and Schmidt, G. (1999) Deamidation of Cdc42 and Rac by Escherichia coli cytotoxic necrotizing factor 1 : activation of c-Jun N-terminal kinase in HeLa cells. Infect Immun 67: 496-503.