Toxin-induced RhoA activity mediates CCL1-triggered signal transducers and activators of transcription protein signaling

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 11183-11194

  Reipschläger, Simone ^a   Kubatzky, Katharina ^b   Taromi, Sanaz ^c   Burger, Meike ^c   Orth, Joachim ^a   Aktories, Klaus ^a   Schmidt, Gudula ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Medical Microbiology and Hygiene   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CYTOKINES; CYTOTOXIC; DEAMIDATION; GTP HYDROLYSIS; GTPASES; INDUCED PROTEINS; KINASE ACTIVATION; PATHOGENIC ESCHERICHIA COLI; PROTEIN SIGNALING; RHO FAMILY; RHO GTPASES; SIGNAL TRANSDUCERS AND ACTIVATORS OF TRANSCRIPTIONS; SIGNALING PATHWAYS; YERSINIA PSEUDOTUBERCULOSIS;

AMINO ACIDS; CHEMICAL ACTIVATION; ESCHERICHIA COLI; HYDROLYSIS; PHOSPHORYLATION;

WELL STIMULATION;

BACTERIAL TOXIN; CCL1 CHEMOKINE; CYTOTOXIC NECROTIZING FACTOR 1; CYTOTOXIC NECROTIZING FACTOR 3; CYTOTOXIC NECROTIZING FACTOR Y; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE P60; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE SILENCING; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIAL TOXINS; CHEMOKINE CCL1; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; JANUS KINASES; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR AP-1;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84859514659     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.313395     Document Type: Article

References (42)

1. Etienne-Manneville, S., and Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635 (Pubitemid 36764489)
2. Mackay, D. J., and Hall, A. (1998) Rho GTPases. J. Biol. Chem. 273, 20685-20688 (Pubitemid 28385341)
3. Kreiselmeier, N. E., Kraynack, N. C., Corey, D. A., and Kelley, T. J. (2003) Statin-mediated correction of STAT1 signaling and inducible nitric-oxide synthase expression in cystic fibrosis epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol 285, L1286-L1295 (Pubitemid 37448800)
4. Loucks, F. A., Le, S. S., Zimmermann, A. K., Ryan, K. R., Barth, H., Aktories, K., and Linseman, D. A. (2006) Rho family GTPase inhibition reveals opposing effects of mitogen-activated protein kinase kinase/extracellular signal-regulated kinase and Janus kinase/signal transducer and activator of transcription signaling cascades on neuronal survival. J. Neurochem. 97, 957-967
5. Bowman, T., Garcia, R., Turkson, J., and Jove, R. (2000) STATs in oncogenesis. Oncogene 19, 2474-2488 (Pubitemid 30339203)
6. Pfeiffer, M., Hartmann, T. N., Leick, M., Catusse, J., Schmitt-Graeff, A., and Burger, M. (2009) Alternative implication of CXCR4 in JAK2/STAT3 activation in small cell lung cancer. Br. J. Cancer 100, 1949-1956
7. Fujimoto, Y., Ochi, H., Maekawa, T., Abe, H., Hayes, C. N., Kumada, H., Nakamura, Y., and Chayama, K. (2011) A single nucleotide polymorphism in activated Cdc42 associated tyrosine kinase 1 influences the interferon therapy in hepatitis C patients. J. Hepatol. 54, 629-639
8. Turkson, J., Bowman, T., Adnane, J., Zhang, Y., Djeu, J. Y., Sekharam, M., Frank, D. A., Holzman, L. B., Wu, J., Sebti, S., and Jove, R. (1999) Requirement for Ras/Rac1-mediated p38 and c-Jun N-terminal kinase signaling in STAT3 transcriptional activity induced by the Src oncoprotein. Mol. Cell. Biol. 19, 7519-7528 (Pubitemid 29493415)
9. Gündogdu, M. S., Liu, H., Metzdorf, D., Hildebrand, D., Aigner, M., Aktories, K., Heeg, K., and Kubatzky, K. F. (2010) The haematopoietic GTPase RhoH modulates IL3 signaling through regulation of STAT activity and IL3 receptor expression. Mol. Cancer 9, 225
10. Schmidt, G., Sehr, P., Wilm, M., Selzer, J., Mann, M., and Aktories, K. (1997) Gln-63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387, 725-729 (Pubitemid 27270615)
11. Flatau, G., Lemichez, E., Gauthier, M., Chardin, P., Paris, S., Fiorentini, C., and Boquet, P. (1997) Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387, 729-733 (Pubitemid 27270616)
12. Hoffmann, C., Pop, M., Leemhuis, J., Schirmer, J., Aktories, K., and Schmidt, G. (2004) The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J. Biol. Chem. 279, 16026-16032 (Pubitemid 38509292)
13. De Rycke, J., Milon, A., and Oswald, E. (1999) Necrotoxic Escherichia coli (NTEC). Two emerging categories of human and animal pathogens. Vet. Res. 30, 221-233 (Pubitemid 129587970)
14. Stoll, T., Markwirth, G., Reipschläger, S., and Schmidt, G. (2009) A new member of a growing toxin family-Escherichia coli cytotoxic necrotizing factor 3 (CNF3). Toxicon 54, 745-753
15. De Rycke, J., González, E. A., Blanco, J., Oswald, E., Blanco, M., and Boivin, R. (1990) Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J. Clin. Microbiol. 28, 694-699 (Pubitemid 20123821)
16. Deleted in proof
17. Sotiropoulos, A., Gineitis, D., Copeland, J., and Treisman, R. (1999) Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169 (Pubitemid 29344904)
18. Dumoutier, L., Tounsi, A., Michiels, T., Sommereyns, C., Kotenko, S. V., and Renauld, J. C. (2004) Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon- λ1. Similarities with type I interferon signaling. J. Biol. Chem. 279, 32269-32274 (Pubitemid 39014676)
19. Dalpke, A. H., Eckerle, S., Frey, M., and Heeg, K. (2003) Triggering of Toll-like receptors modulates IFN-γ signaling. Involvement of serine 727 STAT1 phosphorylation and suppressors of cytokine signaling. Eur. J. Immunol. 33, 1776-1787 (Pubitemid 37120848)
20. Herrmann, A., Vogt, M., Mönnigmann, M., Clahsen, T., Sommer, U., Haan, S., Poli, V., Heinrich, P. C., and Müller-Newen, G. (2007) Nucleocytoplasmic shuttling of persistently activated STAT3. J. Cell Sci. 120, 3249-3261 (Pubitemid 350018416)
21. Sotiropoulos, A., Moutoussamy, S., Renaudie, F., Clauss, M., Kayser, C., Gouilleux, F., Kelly, P. A., and Finidori, J. (1996) Differential activation of Stat3 and Stat5 by distinct regions of the growth hormone receptor. Mol. Endocrinol. 10, 998-1009 (Pubitemid 26268882)
22. Bromberg, J. F., Horvath, C. M., Besser, D., Lathem, W. W., and Darnell, J. E., Jr. (1998) Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18, 2553-2558 (Pubitemid 28183425)
23. Orth, J. H., Aktories, K., and Kubatzky, K. F. (2007) Modulation of host cell gene expression through activation of STAT transcription factors by Pasteurella multocida toxin. J. Biol. Chem. 282, 3050-3057 (Pubitemid 47084349)
24. Koch, G., Benz, C., Schmidt, G., Olenik, C., and Aktories, K. (1997) Role of Rho protein in lovastatin-induced breakdown of actin cytoskeleton. J. Pharmacol. Exp. Ther. 283, 901-909 (Pubitemid 27514653)
25. Kortylewski, M., Jove, R., and Yu, H. (2005) Targeting STAT3 affects melanoma on multiple fronts. Cancer Metastasis Rev. 24, 315-327 (Pubitemid 40922802)
26. Blumenthal, B., Hoffmann, C., Aktories, K., Backert, S., and Schmidt, G. (2007) The cytotoxic necrotizing factors from Yersinia pseudotuberculosis and from Escherichia coli bind to different cellular receptors but take the same route to the cytosol. Infect. Immun. 75, 3344-3353 (Pubitemid 47040935)
27. Ongusaha, P. P., Qi, H. H., Raj, L., Kim, Y. B., Aaronson, S. A., Davis, R. J., Shi, Y., Liao, J. K., and Lee, S. W. (2008) Identification of ROCK1 as an upstream activator of the JIP-3 to JNK signaling axis in response to UVB damage. Sci. Signal 1, ra14
28. Marinissen, M. J., Chiariello, M., Tanos, T., Bernard, O., Narumiya, S., and Gutkind, J. S. (2004) The small GTP-binding protein RhoA regulates c-jun by a ROCK-JNK signaling axis. Mol. Cell 14, 29-41 (Pubitemid 38469907)
29. q/11-selective inhibitor. J. Biol. Chem. 279, 47438-47445
30. Orth, J. H., Lang, S., Taniguchi, M., and Aktories, K. (2005) Pasteurella multocida toxin-induced activation of RhoA is mediated via two families of Gα proteins, Gαq and Gα12/13. J. Biol. Chem. 280, 36701-36707 (Pubitemid 41587748)
31. Darnell, J. E., Jr. (1997) STATs and gene regulation. Science 277, 1630-1635
32. Yue, P., and Turkson, J. (2009) Targeting STAT3 in cancer. How successful are we? Expert. Opin. Investig. Drugs 18, 45-56
33. Raptis, L., Arulanandam, R., Geletu, M., and Turkson, J. (2011) The R(h)oads to Stat3. Stat3 activation by the Rho GTPases. Exp. Cell Res. 317, 1787-1795
34. Lee, S. J., Qin, H., and Benveniste, E. N. (2007) Simvastatin inhibits IFN- γ-induced CD40 gene expression by suppressing STAT-1α. J. Leukoc. Biol. 82, 436-447 (Pubitemid 47230655)
35. Banes-Berceli, A. K., Shaw, S., Ma, G., Brands, M., Eaton, D. C., Stern, D. M., Fulton, D., Caldwell, R. W., and Marrero, M. B. (2006) Effect of simvastatin on high glucose- and angiotensin II-induced activation of the JAK/STAT pathway in mesangial cells. Am. J. Physiol. Renal Physiol. 291, F116-F121 (Pubitemid 43945941)
36. 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 (Pubitemid 29059179)
37. Tiffany, H. L., Lautens, L. L., Gao, J. L., Pease, J., Locati, M., Combadiere, C., Modi, W., Bonner, T. I., and Murphy, P. M. (1997) Identification of CCR8. A human monocyte and thymus receptor for the CC chemokine I-309. J. Exp. Med. 186, 165-170 (Pubitemid 27304860)
38. Haque, N. S., Fallon, J. T., Pan, J. J., Taubman, M. B., and Harpel, P. C. (2004) Chemokine receptor-8 (CCR8) mediates human vascular smooth muscle cell chemotaxis and metalloproteinase-2 secretion. Blood 103, 1296-1304 (Pubitemid 38168640)
39. Homey, B., Meller, S., Savinko, T., Alenius, H., and Lauerma, A. (2007) Modulation of chemokines by staphylococcal superantigen in atopic dermatitis. Chem. Immunol. Allergy 93, 181-194 (Pubitemid 46924878)
40. Choi, Y. B., and Nicholas, J. (2008) Autocrine and paracrine promotion of cell survival and virus replication by human herpesvirus 8 chemokines. J. Virol. 82, 6501-6513
41. Emdad, L., Lebedeva, I. V., Su, Z. Z., Gupta, P., Sauane, M., Dash, R., Grant, S., Dent, P., Curiel, D. T., Sarkar, D., and Fisher, P. B. (2009) Historical perspective and recent insights into our understanding of the molecular and biochemical basis of the antitumor properties of mda-7/IL-24. Cancer Biol. Ther. 8, 391-400
42. Ouyang, W., Rutz, S., Crellin, N. K., Valdez, P. A., and Hymowitz, S. G. (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 29, 71-109