Smurf1 protein negatively regulates interferon-γ signaling through promoting STAT1 protein ubiquitination and degradation

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17006-17015

  Yuan, Chao ^a   Qi, Jianni ^a   Zhao, Xueying ^a   Gao, Chengjiang ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-PROLIFERATIVE; ANTI-TUMORS; AUTOIMMUNE DISEASE; CYTOKINES; IMMUNE RESPONSE; NEGATIVE FEEDBACK REGULATORS; NEGATIVE REGULATORS; OVER-EXPRESSION; POLYUBIQUITINATION; PROTEASOMAL DEGRADATION; SERINE PHOSPHORYLATION; TARGET GENES; UBIQUITINATION; WW DOMAIN;

AMINO ACIDS; ANTIBIOTICS; GENE EXPRESSION; GLYCOPROTEINS; IMMUNOLOGY; INTERFERONS; PHOSPHORYLATION; SIGNALING;

DEGRADATION;

GAMMA INTERFERON; STAT1 PROTEIN;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOREGULATION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; VESICULAR STOMATITIS VIRUS;

AMINO ACID MOTIFS; ANIMALS; HEK293 CELLS; HUMANS; INTERFERON-GAMMA; MACROPHAGES, PERITONEAL; MICE; NIH 3T3 CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; STAT1 TRANSCRIPTION FACTOR; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VIRUS DISEASES;

EID: 84861210911     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.341198     Document Type: Article

References (32)

1. Zhu, H., Kavsak, P., Abdollah, S., Wrana, J. L., and Thomsen, G. H. (1999) A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693
2. Ebisawa, T., Fukuchi, M., Murakami, G., Chiba, T., Tanaka, K., Imamura, T., and Miyazono, K. (2001) Smurf1 interacts with transforming growth factor-β type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276, 12477-12480
3. Wang, H. R., Zhang, Y., Ozdamar, B., Ogunjimi, A. A., Alexandrova, E., Thomsen, G. H., and Wrana, J. L. (2003) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302, 1775-1779 (Pubitemid 37505743)
4. Yamashita, M., Ying, S. X., Zhang, G. M., Li, C., Cheng, S. Y., Deng, C. X., and Zhang, Y. E. (2005) Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121, 101-113
5. Narimatsu, M., Bose, R., Pye, M., Zhang, L., Miller, B., Ching, P., Sakuma, R., Luga, V., Roncari, L., Attisano, L., and Wrana, J. L. (2009) Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137, 295-307
6. Zhao, L., Huang, J., Guo, R., Wang, Y., Chen, D., and Xing, L. (2010) Smurf1 inhibits mesenchymal stem cell proliferation and differentiation into osteoblasts through JunB degradation. J. Bone Miner. Res. 25, 1246-1256
7. Li, S., Lu, K., Wang, J., An, L., Yang, G., Chen, H., Cui, Y., Yin, X., Xie, P., Xing, G., He, F., and Zhang, L. (2010) Ubiquitin ligase Smurf1 targets TRAF family proteins for ubiquitination and degradation. Mol. Cell Biochem. 338, 11-17
8. Lee, Y. S., Park, J. S., Kim, J. H., Jung, S. M., Lee, J. Y., Kim, S. J., and Park, S. H. (2011) Smad6-specific recruitment of Smurf E3 ligases mediates TGF-β1-induced degradation of MyD88 in TLR4 signaling. Nat. Commun. 2, 460
9. van Boxel-Dezaire, A. H., Rani, M. R., and Stark, G. R. (2006) Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25, 361-372 (Pubitemid 44354225)
10. Schroder, K., Hertzog, P. J., Ravasi, T., and Hume, D. A. (2004) Interferon- γ: an overview of signals, mechanisms, and functions. J. Leukoc. Biol. 75, 163-189 (Pubitemid 38174573)
11. Ramana, C. V., Chatterjee-Kishore, M., Nguyen, H., and Stark, G. R. (2000) Complex roles of Stat1 in regulating gene expression. Oncogene 19, 2619-2627 (Pubitemid 30339218)
12. Meraz, M. A., White, J. M., Sheehan, K. C., Bach, E. A., Rodig, S. J., Dighe, A. S., Kaplan, D. H., Riley, J. K., Greenlund, A. C., Campbell, D., Carver- Moore, K., DuBois, R. N., Clark, R., Aguet, M., and Schreiber, R. D. (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442 (Pubitemid 26058568)
13. Ramana, C. V., Gil, M. P., Schreiber, R. D., and Stark, G. R. (2002) Stat1- dependent and -independent pathways in IFN-γ-dependent signaling. Trends Immunol. 23, 96-101
14. Krämer, O. H., Knauer, S. K., Greiner, G., Jandt, E., Reichardt, S., Gührs, K. H., Stauber, R. H., Böhmer, F. D., and Heinzel, T. (2009) A phosphorylation- acetylation switch regulates STAT1 signaling. Genes Dev. 23, 223-235
15. Tanaka, T., Soriano, M. A., and Grusby, M. J. (2005) SLIM is a nuclear ubiquitin E3 ligase that negatively regulatesSTATsignaling. Immunity 22, 729-736 (Pubitemid 40814503)
16. Zhao, W., Wang, L., Zhang, L., Yuan, C., Kuo, P. C., and Gao, C. (2010) Differential expression of intracellular and secreted osteopontin isoforms by murine macrophages in response to Toll-like receptor agonists. J. Biol. Chem. 285, 20452-20461
17. Gao, C., Guo, H., Mi, Z., Grusby, M. J., and Kuo, P. C. (2007) Osteopontin induces ubiquitin-dependent degradation of STAT1 in RAW264.7 murine macrophages. J. Immunol. 178, 1870-1881 (Pubitemid 46154660)
18. An, H., Zhao, W., Hou, J., Zhang, Y., Xie, Y., Zheng, Y., Xu, H., Qian, C., Zhou, J., Yu, Y., Liu, S., Feng, G., and Cao, X. (2006) SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity 25, 919-928 (Pubitemid 44894946)
19. Liu, B., Mink, S., Wong, K. A., Stein, N., Getman, C., Dempsey, P. W., Wu, H., and Shuai, K. (2004) PIAS1 selectively inhibits interferon-inducible genes and is important in innate immunity. Nat. Immunol. 5, 891-898 (Pubitemid 39276233)
20. Mao, A. P., Li, S., Zhong, B., Li, Y., Yan, J., Li, Q., Teng, C., and Shu, H. B. (2010) Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-β (IFN-β) and cellular antiviral response. J. Biol. Chem. 285, 9470-9476
21. Zheng, Y., An, H., Yao, M., Hou, J., Yu, Y., Feng, G., and Cao, X. (2010) Scaffolding adaptor protein Gab1 is required for TLR3/4- and RIG-I-mediated production of proinflammatory cytokines and type I IFN in macrophages. J. Immunol. 184, 6447-6456
22. Xing, L., Zhang, M., and Chen, D. (2010) Smurf control in bone cells. J. Cell. Biochem. 110, 554-563
23. Eilers, A., Georgellis, D., Klose, B., Schindler, C., Ziemiecki, A., Harpur, A. G., Wilks, A. F., and Decker, T. (1995) Differentiation-regulated serine phosphorylation of STAT1 promotes GAF activation in macrophages. Mol. Cell. Biol. 15, 3579-3586
24. Barrios-Rodiles, M., Brown, K. R., Ozdamar, B., Bose, R., Liu, Z., Donovan, R. S., Shinjo, F., Liu, Y., Dembowy, J., Taylor, I. W., Luga, V., Przulj, N., Robinson, M., Suzuki, H., Hayashizaki, Y., Jurisica, I., and Wrana, J. L. (2005) High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307, 1621-1625 (Pubitemid 40354744)
25. Chong, P. A., Lin, H., Wrana, J. L., and Forman-Kay, J. D. (2010) Coupling of tandem Smad ubiquitination regulatory factor (Smurf) WW domains modulates target specificity. Proc. Natl. Acad. Sci. U.S.A. 107, 18404-18409
26. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
27. Wen, Z., Zhong, Z., and Darnell, J. E., Jr. (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250
28. Horvath, C. M., and Darnell, J. E., Jr. (1996) The antiviral state induced by α-interferon and γ-interferon requires transcriptionally active Stat1 protein. J. Virol. 70, 647-650 (Pubitemid 126508840)
29. Schindler, C. W. (2002) Series introduction: JAK-STAT signaling in human disease. J. Clin. Invest. 109, 1133-1137
30. Kim, T. K., and Maniatis, T. (1996) Regulation of interferon-γ- activated STAT1 by the ubiquitin-proteasome pathway. Science 273, 1717-1719 (Pubitemid 26317788)
31. Kubota, T., Yokosawa, N., Yokota, S., Fujii, N., Tashiro, M., and Kato, A. (2005) Mumps virus V protein antagonizes interferon without the complete degradation of STAT1. J. Virol. 79, 4451-4459 (Pubitemid 40388382)
32. Didcock, L., Young, D. F., Goodbourn, S., and Randall, R. E. (1999) The V protein of simian virus 5 inhibits interferon signaling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73, 9928-9933