Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis

Molecular Microbiology

Volumn 47, Issue 5, 2003, Pages 1305-1315

  Viboud, Gloria I ^a   So, Stephane Shu Kin ^a   Ryndak, Michelle B ^a   Bliska, James B ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; GUANOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; INVASIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN YOPB; PROTEIN YOPD; PROTEIN YOPH; PROTEIN YOPJ; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL ADHESION; CHANNEL GATING; CYTOKINE PRODUCTION; EPITHELIUM CELL; GENE TRANSLOCATION; GENETIC COMPLEMENTATION; HELA CELL; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE; YERSINIA PSEUDOTUBERCULOSIS;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; INFLAMMATION; INTERLEUKIN-8; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM PROTEINS; NF-KAPPA B; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN TRANSPORT; PROTEIN-TYROSINE-PHOSPHATASE; RAS PROTEINS; RHO GTP-BINDING PROTEINS; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0037338674     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03350.x     Document Type: Article

References (50)

1. 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.
2. Black, D.S., and Bliska, J.B. (2000) The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol Microbiol 37: 515-527.
3. Black, D.S., Montagna, L.G., Zitsmann, S., and Bliska, J.B. (1998) Identification of an amino-terminal substrate-binding domain in the Yersinia tyrosine phosphatase that is required for efficient recognition of focal adhesion targets. Mol Microbiol 29: 1263-1274.
4. Bliska, J.B. (2000) Yop effectors of Yersinia spp. and actin rearrangements. Trends Microbiol 8: 205-208.
5. 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.
6. Bölin, I., Norlander, L., and Wolf-Watz, H. (1982) Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun 37: 506-512.
7. Buttner, D., and Bonas, U. (2002) Port of entry - the type III secretion translocon. Trends Microbiol 10: 186-192.
8. Cornelis, G.R., Boland, A., Boyd, A.P., Geuijen, C., Iriarte, M., Neyt, C., et al. (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62: 1315-1352.
9. Coso, O.A., Chiariello, M., Yu, J.C., Teramoto, H., Crespo, P., Xu, N., et al. (1995) The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81: 1137-1146.
10. Czerucka, D., Dahan, S., Mograbi, B., Rossi, B., and Rampal, P. (2001) Implication of mitogen-activated protein kinases in T84 cell responses to enteropathogenic Escherichia coli' infection. Infect Immun 69: 1298-1305.
11. Didierlaurent, A., Sirard, J.C., Kraehenbuhl, J.P., and Neutra, M.R. (2002) How the gut senses its content. Cell Microbiol 4: 61-72.
12. Dragneva, Y., Anuradha, C.D., Valeva, A., Hoffmann, A., Bhakdi, S., and Husmann, M. (2001) Subcytocidal attack by staphylococcal alpha-toxin activates NF-kappaB and induces interleukin-8 production. Infect Immun 69: 2630-2635.
13. Frost, J.A., Steen, H., Shapiro, P., Lewis, T., Ahn, N., Shaw, P.E., and Cobb, M.H. (1997) Cross-cascade activation of ERKs and ternary complex factors by Rho family members. EMBO J 16: 6426-6438.
14. Galán, J.E., and Bliska, J.B. (1996) Cross-talk between bacterial pathogens and their host cells. Annu Rev Cell Dev Biol 12: 221-255.
15. de Grado, M., Rosenberger, C.M., Gauthier, A., Vallance, B.A., and Finlay, B.B. (2001) Enteropathogenic Escherichia coli infection induces expression of the early growth response factor by activating mitogen-activated protein kinase cascades in epithelial cells. Infect Immun 69: 6217-6224.
16. Håkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homblé, F., and Wolf-Watz, H. (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.
17. Holmström, A., Olsson, J., Cherepanov, P., Maier, E., Nordfelth, R., Pettersson, J., et al. (2001) LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol Microbiol 39: 620-632.
18. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
19. Isberg, R.R., and Barnes, P. (2001) Subversion of integrins by enteropathogenic Yersinia. J Cell Sci 114: 21-28.
20. Juris, S.J., Shao, F., and Dixon, J.E. (2002) Yersinia effectors target mammalian signalling pathways. Cell Microbiol 4: 201-211.
21. Kolch, W. (2000) Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem J 351: 289-305.
22. Li, W., Chong, H., and Guan, K.L. (2001) Function of the Rho family GTPases in Ras-stimulated Raf activation. J Biol Chem 276: 34728-34737.
23. Li, X., and Stark, G.R. (2002) NFkappaB-dependent signaling pathways. Exp Hematol 30: 285-296.
24. Mukaida, N., Okamoto, S., Ishikawa, Y., and Matsushima, K. (1994) Molecular mechanism of interleukin-8 gene expression. J Leukoc Biol 56: 554-558.
25. Neyt, C., and Cornelis, G.R. (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33: 971-981.
26. Orth, K. (2002) Function of the Yersinia effector YopJ. Curr Opin Microbiol 5: 38-43.
27. Orth, K., Xu, Z., Mudgett, M.B., Bao, Z.Q., Palmer, L.E., Bliska, J.B., et al. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
28. Palmer, L.E., Hobbie, S., Galán, J.E., and Bliska, J.B. (1998) YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and down-regulation of the MAP kinases p38 and JNK. Mol Microbiol 27: 953-965.
29. Palmer, L.E., Pancetti, A.R., Greenberg, S., and Bliska, J.B. (1999) YopJ of Yersinia spp. is sufficient to cause down-regulation of multiple mitogen-activated protein kinases in eukaryotic cells. Infect Immun 67: 708-716.
30. Persson, C., Nordfelth, R., Holmström, A., Hakånsson, S., Rosqvist, R., and Wolf-Watz, H. (1995) Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol Microbiol 18: 135-150.
31. Persson, C., Carballeira, N., Wolf-Watz, H., and Fällman, M. (1997) The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J 16: 2307-2318.
32. Pettersson, J., Holmström, A., Hill, J., Leary, S., Frithz-Lindsten, E., von Euler-Matell, A., et al. (1999) The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 32: 961-976.
33. Plano, G.V., Day, J.B., and Ferracci, F. (2001) Type III export: new uses for an old pathway. Mol Microbiol 40: 284-293.
34. Ruckdeschel, K., Harb, S., Roggenkamp, A., Hornef, M., Zumbihl, R., Kohler, S., et al. (1998) Yersinia enterocolitica impairs activation of transcription factor NF-κB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor a production. J Exp Med 187: 1069-1079.
35. Sarker, M.R., Neyt, C., Stainier, I., and Cornelis, G.R. (1998) The Yersinia Yop virulon: LcrV is required for extrusion of the translocators YopB and YopD. J Bacteriol 180: 1207-1214.
36. Sauvonnet, N., Lambermont, I., Bruggen Pv.P., and Cornelis, G.R. (2002) YopH prevents monocyte chemoattractant protein 1 expression in macrophages and T-cell proliferation through inactivation of the phosphatidylinositol 3-kinase pathway. Mol Microbiol 45: 805-815.
37. Schesser, K., Spiik, A.K., Dukuzumuremyi, J.M., Neurath, M.F., Pettersson, S., and Wolf-Watz, H. (1998) The yopJ locus is required for Yersinia-mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol 28: 1067-1079.
38. Schulte, R., and Autenrieth, I.B. (1998) Yersinia enterocolitica-induced intedeukin-8 secretion by human intestinal epithelial cells depends on cell differentiation. Infect Immun 66: 1216-1224.
39. Schulte, R., Wattiau, P., Hartland, E.L., Robins-Browne, R.M., and Cornelis, G.R. (1996) Differential secretion of interleukin-8 by human epithelial cell lines upon entry of virulent or nonvirulent Yersinia enterocolitica. Infect Immun 64: 2106-2113.
40. Schulte, R., Zumbihl, R., Kampik, D., Fauconnier, A., and Autenrieth, I.B. (1998) Wortmannin blocks Yersinia invasin-triggered internalization, but not interleukin-8 production by epithelial cells. Med Microbiol Immunol (Berlin) 187: 53-60.
41. Schulte, R., Grassl, G.A., Preger, S., Fessele, S., Jacobi, C.A., Schaller, M., et al. (2000) Yersinia enterocolitica invasin protein triggers IL-8 production in epithelial cells via activation of Rel p65-p65 homodimers. FASEB J 14: 1471-1484.
42. Shao, F., Merrit, P.M., Bao, Z., Innes, R.W., and Dixon, J.E. (2002) A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109: 575-588.
43. Simonet, M., and Falkow, S. (1992) Invasin expression in Yersinia pseudotuberculosis. Infect Immun 60: 4414-4417.
44. Sizemore, N., Leung, S., and Stark, G.R. (1999) Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol Cell Biol 19: 4798-4805.
45. Tardy, F., Homblé, F., Neyt, C., Wattiez, R., Cornelis, G.R., Ruysschaert, J.M., and Cabiaux, V. (1999) Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J 18: 6793-6799.
46. Viboud, G.I., and Bliska, J.B. (2001) A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J 20: 5373-5382.
47. Von Pawel-Rammingen, U., Telepnev, M.V., Schmidt, G., Aktories, K., Wolf-Watz, H., and Rosqvist, R. (2000) GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol Microbiol 36: 737-748.
48. Walev, I., Hombach, M., Bobkiewicz, W., Fenske, D., Bhakdi, S., and Husmann, M. (2002) Resealing of large transmembrane pores produced by streptolysin O in nucleated cells is accompanied by NF-kappaB activation and downstream events. FASEB J 16: 237-239.
49. Yao, T., Mecsas, J., Healy, J.l., Falkow, S., and Chien, Y. (1999) Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, YopH. J Exp Med 190: 1343-1350.
50. Zumbihl, R., Aepfelbacher, M., Andor, A., Jacobi, C.A., Ruckdeschel, K., Rouot, B., and Heesemann, J. (1999) The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J Biol Chem 274: 29289-29293.