Suppressor of cytokine signaling 1 inhibits IFN-γ inflammatory signaling in human keratinocytes by sustaining ERK1/2 activation

FASEB Journal

Volumn 22, Issue 9, 2008, Pages 3287-3297

  Madonna, Stefania ^a   Scarponi, Claudia ^a   De Pità, Ornella ^a   Albanesi, Cristina ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Antiinflammatory pathways; P120RasGAP; RAF 1; RAS; Skin immune responses; Skin inflammation

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; RAF PROTEIN; RAS PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1;

ARTICLE; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; INFLAMMATION; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CXCL10; ENZYME ACTIVATION; HUMANS; INTERFERON TYPE II; INTERLEUKIN-8; KERATINOCYTES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; P120 GTPASE ACTIVATING PROTEIN; RAS PROTEINS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UP-REGULATION;

EID: 51349169485     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.08-106831     Document Type: Article

References (37)

1. Bos, J. D., de Rie, M. A., Teunissen, M. B., and Piskin, G. (2006) Psoriasis: dysregulation of innate immunity. Br. J. Dermatol. 152, 1098-1107
2. Albanesi, C., Scarponi, C., Giustizieri, M. L., and Girolomoni, G. (2005) Keratinocytes in inflammatory skin diseases. Curr. Drug Targets Inflamm. Allergy 4, 329-334
3. Albanesi, C., Cavani, A., and Girolomoni, G. (1999) IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonistic effects with IFN-γ and TNF-α. J. Immunol. 162, 494-502
4. Albanesi, C., Scarponi, C., Sebastiani, S., Cavani, A., Federici, M., De Pità, O., Puddu, P., and Girolomoni, G. (2000) IL-4 enhances keratinocyte expression of CXCR3 agonistic chemokines. J. Immunol. 165, 1395-1402
5. Zhang, X., Chen, X., Song, H., Chen, H. Z., and Rovin, B. H. (2005) Activation of the Nrf2/antioxidant response pathway increases IL-8 expression. Eur. J. Immunol. 35, 3258-3267
6. Gillitzer, R., and Goebeler, M. (2001) Chemokines in cutaneous wound healing. J. Leukoc. Biol. 69, 513-521
7. Li, A., Dubey, S., Varney, M. L., Dave, B. J., and Singh, R. K. (2003) IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J. Immunol. 170, 3369-3376
8. Platanias, L. C. (2005) Mechanisms of type-I- and type-II-interferon- mediated signalling. Nat. Rev. Immunol. 5, 375-385
9. Goh, K. C., Haque, S. J., and Williams, B. R. (1999) p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons. EMBO J. 18, 5601-5608
10. Nguyen, V. A., Chen, J., Hong, F., Ishac, E. J., and Gao, B. (2000) Interferons activate the p42/44 mitogen-activated protein kinase and JAK-STAT (Janus kinase-signal transducer and activator transcription factor) signalling pathways in hepatocytes: differential regulation by acute ethanol via a protein kinase C-dependent mechanism. Biochem. J. 349, 427-434
11. Takaoka, A., Tanaka, N., Mitani, Y., Miyazaki, T., Fujii, H., Sato, M., Kovarik, P., Decker, T., Schlessinger, J., and Taniguchi, T. (1999) Protein tyrosine kinase Pyk2 mediates the Jak-dependent activation of MAPK and Stat1 in IFN-gamma, but not IFN-alpha, signaling. EMBO J. 18, 2480-2488
12. Nguyen, H., Ramana, C. V., Bayes, J., and Stark, G. R. (2001) Roles of phosphatidylinositol 3-kinase in interferon-γ-dependent phosphorylation of STAT1 on serine 727 and activation of gene expression J. Biol. Chem. 276, 33361-33368
13. 2+ and CaMKII for Stat1 Ser-727 phosphorylation in response to IFN-γ. Proc. Natl. Acad. Sci. U. S. A. 99, 5971-5976
14. Hu, J., Roy, S. K., Shapiro, P. S., Rodig, S. R., Reddy, S. P., Platanias, L. C., Schreiber, R. D., and Kalvakolanu, D. V. (2001) ERK1 and ERK2 activate CCAAAT/enhancer-binding protein-beta-dependent gene transcription in response to interferon-gamma. J. Biol. Chem. 276, 287-297
15. Gough, D. J., Sabapathy, K., Ko, E. Y., Arthur, H. A., Schreiber, R. D., Trapani, J. A., Clarke, C. J., and Johnstone, R. W. (2007) A novel c-Jun-dependent signal transduction pathway necessary for the transcriptional activation of interferon-γ response genes. J. Biol. Chem. 282, 938-946
16. Ala-aho, R., Johansson, N., Grénman, R., Fusenig, N. E., López-Otín, C., and Kähäri, V. M. (2000) Inhibition of collagenase-3 (MMP-13) expression in transformed human keratinocytes by interferon-gamma is associated with activation of extracellular signal-regulated kinase-1,2 and STAT1. Oncogene 13, 248-257
17. Ramana, C. V., Gil, M. P., Schreiber, R. D., and Stark, G. R. (2002) Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol. 23, 96-101
18. Mascia, F., Mariani, V., Girolomoni, G., and Pastore, S. (2003) Blockade of the EGF receptor induces a deranged chemokine expression in keratinocytes leading to enhanced skin inflammation. Am. J. Pathol. 163, 303-312
19. Pastore, S., Mascia, F., Mariotti, F., Dattilo, C., Mariani, V., and Girolomoni, G. (2005) ERK1/2 regulates epidermal chemokine expression and skin inflammation. J. Immunol. 174, 5047-5056
20. Federici, M., Giustizieri, M. L., Scarponi, C., Girolomoni, G., and Albanesi, C. (2002) Impaired IFN-gamma-dependent inflammatory responses in human keratinocytes overexpressing the suppressor of cytokine signaling 1. J. Immunol. 169, 434-442
21. Knisz, J., and Rothman, P. B. (2007) Suppressor of cytokine signaling in allergic inflammation. J. Allergy Clin. Immunol. 119, 739-745
22. Yoshimura, A., Naka, T., and Kubo, M. (2007) SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7, 454-465
23. Cacalano, N. A., Sanden, D., and Johnston, J. A. (2001) Tyrosine-phosphorylated SOCS-3 inhibits STAT activation but binds to p120 RasGAP and activates Ras. Nat. Cell Biol. 3, 460-465
24. Wang, D., Li, Z., Messing, E. M., and Wu, G. (2005) The SPRY domain-containing SOCS box protein 1 (SSB-1) interacts with MET and enhances the hepatocyte growth factor-induced Erk-Elk-1-serum response element pathway J. Biol. Chem. 280, 16393-16401
25. Ben-Zvi, T., Yayon, A., Gertler, A., and Monsonego-Ornan, E. (2006) Suppressors of cytokine signaling (SOCS) 1 and SOCS3 interact with and modulate fibroblast growth factor receptor signalling 1. J. Cell Sci. 119, 380-387
26. Han, Y., He, T., Huang, D., Pardo, C. A., and Ransohoff, R. M. (2001) TNF-α mediates SDF-1α-induced NF-κB activation and cytotoxic effects in primary astrocytes. J. Clin. Invest. 108, 425-435
27. Sah, J. F., Eckert, R. L., Chandraratna, R. A. S., and Rorke, E. A. (2002) Retinoids suppress epidermal growth factor-associated cell proliferation by inhibiting epidermal growth factor receptor-dependent ERK1/2 activation. J. Biol. Chem. 277, 9728-9735
28. Porcile, C., Bajetto, A., Barbieri, F., Barbero, S., Bonavia, R., Biglieri, M., Pirani, P., Florio, T., and Schettini, G. (2005) Stromal cell-derived factor-1a (SDF-1a/CXCL12) stimulates ovarian cancer cell growth through the EGF receptor transactivation. Exp. Cell Res. 308, 241-253
29. Hilton, D. J., Richardson, R. T., Alexander, W. S., Viney, E. M., Willson, T. A., Sprigg, N. S., Starr, R., Nicholson, S. E., Metcalf, D., and Nicola, N. A. (1998) Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. U. S. A. 95, 114-119
30. He, Y., Zhang, W., Zhang, R., Zhang, H., and Min, W. (2006) SOCS1 inhibits tumor necrosis factor-induced activation of ASK1-JNK inflammatory signaling by mediating ASK1 degradation. J. Biol. Chem. 281, 5559-5566
31. Mansell, A., Smith, R., Doyle, S. L., Gray, P., Fenner, J. E., Crack, P. J., Nicholson, S. E., Hilton, D. J., O'Neill, L. A., and Hertzog, P. J. (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat. Immunol. 7, 148-155
32. De Sepulveda, P., Ilangumaran, S., and Rottapel, R. (2000) Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation. J. Biol. Chem. 275, 14005-14008
33. Ungureanu, D., Saharinen, P., Junttila, I., Hilton, D. J., and Silvennoinen, O. (2002) Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol. Cell Biol. 22, 3316-3326
34. Dajee, M., Tarutani, M., Deng, H., Cai, T., and Khavari, P. A. (2002) Epidermal Ras blockade demonstrates spatially localized Ras promotion of proliferation and inhibition of differentiation. Oncogene 21, 1527-1538
35. Van der Geer, P., Henkemeyer, M., Jacks, T., and Pawson, T. (1997) Aberrant Ras regulation and reduced p190 tyrosine phosphorylation in cells lacking p120-Gap. Mol. Cell Biol. 17, 1840-1847
36. Waiboci, L. W., Ahmed, C. M., Mujtaba, M. G., Flowers, L. O., Martin, J. P., Haider, M. I., and Johnson, H. M. (2007) Both the suppressor of cytokine signaling 1 (SOCS-1) kinase inhibitory region and SOCS-1 mimetic bind to JAK2 autophosphorylation site: implications for the development of a SOCS-1 antagonist. J. Immunol. 178, 5058-5068
37. Mujtaba, M. G., Flowers, L. O., Patel, C. B., Haider, M. I., and Johnson, H. M. (2005) Treatment of mice with the suppressor of cytokine signaling-1 mimetic peptide, tyrosine kinase inhibitor peptide, prevents development of the acute form of experimental allergic encephalomyelitis and induces stable remission in the chronic relapsing/remitting form. J. Immunol. 175, 5077-5086