Ubiquitination regulates expression of the serine/argininerich splicing factor 1 (SRSF1) in normal and systemic lupus erythematosus (SLE) t cells

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 4126-4134

  Moulton, Vaishali R ^a   Gillooly, Andrew R ^a   Tsokos, George C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNITY; IMMUNOLOGY; PROTEASOME; PROTEIN TURNOVER; T CELL; T CELL RECEPTOR; UBIQUITIN;

ANTIGENS, CD28; ANTIGENS, CD3; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RNA, MESSENGER; RNA-BINDING PROTEINS; T-LYMPHOCYTES; UBIQUITINATION;

EID: 84894144703     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.518662     Document Type: Article

References (37)

1. Tsokos, G. C. (2011) Systemic lupus erythematosus. N. Engl. J. Med. 365, 2110-2121
2. Linker-Israeli, M., Bakke, A. C., Kitridou, R. C., Gendler, S., Gillis, S., and Horwitz, D. A. (1983) Defective production of interleukin 1 and interleukin 2 in patients with systemic lupus erythematosus (SLE). J. Immunol. 130, 2651-2655
3. Moulton, V. R., and Tsokos, G. C. (2011) Abnormalities of T cell signaling in systemic lupus erythematosus. Arthritis Res. Ther. 13, 207
4. Perl, A. (2010) Pathogenic mechanisms in systemic lupus erythematosus. Autoimmunity 43, 1-6
5. Brundula, V., Rivas, L. J., Blasini, A. M., París, M., Salazar, S., Stekman, I. L., and Rodríguez, M. A. (1999) Diminished levels of T cell receptor chains in peripheral blood T lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 42, 1908-1916
6. Nambiar, M. P., Mitchell, J. P., Ceruti, R. P., Malloy, M. A., and Tsokos, G. C. (2003) Prevalence of T cell receptor chain deficiency in systemic lupus erythematosus. Lupus 12, 46-51
7. Moulton, V. R., Kyttaris, V. C., Juang, Y. T., Chowdhury, B., and Tsokos, G. C. (2008) The RNA-stabilizing protein HuR regulates the expression of chain of the human T cell receptor-associated CD3 complex. J. Biol. Chem. 283, 20037-20044
8. Moulton, V. R., and Tsokos, G. C. (2010) Alternative splicing factor/splicing factor 2 regulates the expression of the subunit of the human T cell receptor-associated CD3 complex. J. Biol. Chem. 285, 12490-12496
9. Moulton, V. R., Grammatikos, A. P., Fitzgerald, L. M., and Tsokos, G. C. (2013) Splicing factor SF2/ASF rescues IL-2 production in T cells from systemic lupus erythematosus patients by activating IL-2 transcription. Proc. Natl. Acad. Sci. U.S.A. 110, 1845-1850
10. Black, D. L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72, 291-336
11. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J. L., and Lafyatis, R. (2002) Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev. 16, 594-607
12. Sun, D., Novotny, M., Bulek, K., Liu, C., Li, X., and Hamilton, T. (2011) Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat. Immunol. 12, 853-860
13. Michlewski, G., Sanford, J. R., and Cáceres, J. F. (2008) The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol. Cell 30, 179-189
14. Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S., and Fu, X. D. (2008) The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15, 819-826
15. Martinez, N. M., and Lynch, K. W. (2013) Control of alternative splicing in immune responses: many regulators, many predictions, much still to learn. Immunol. Rev. 253, 216-236
16. Matter, N., Herrlich, P., and König, H. (2002) Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 420, 691-695
17. Motta-Mena, L. B., Heyd, F., and Lynch, K. W. (2010) Context-dependent regulatory mechanism of the splicing factor hnRNP L. Mol. Cell 37, 223-234
18. Valitutti, S., Müller, S., Salio, M., and Lanzavecchia, A. (1997) Degradation of T cell receptor (TCR)-CD3 complexes after antigenic stimulation. J. Exp. Med. 185, 1859-1864
19. Baeuerle, P. A., and Baltimore, D. (1988) IB: a specific inhibitor of the NF-κB transcription factor. Science 242, 540-546
20. Chen, Z., Hagler, J., Palombella, V. J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. (1995) Signal-induced site-specific phosphorylation targets IB to the ubiquitin-proteasome pathway. Genes Dev. 9, 1586-1597
21. Bronevetsky, Y., Villarino, A. V., Eisley, C. J., Barbeau, R., Barczak, A. J., Heinz, G. A., Kremmer, E., Heissmeyer, V., McManus, M. T., Erle, D. J., Rao, A., and Ansel, K. M. (2013) T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J. Exp. Med. 210, 417-432
22. Breig, O., and Baklouti, F. (2013) Proteasome-mediated proteolysis of SRSF5 splicing factor intriguingly co-occurs with SRSF5 mRNA upregulation during late erythroid differentiation. PLoS One 8, e59137
23. Scharschmidt, E., Wegener, E., Heissmeyer, V., Rao, A., and Krappmann, D. (2004) Degradation of Bcl10 induced by T-cell activation negatively regulates NF-κB signaling. Mol. Cell. Biol. 24, 3860-3873
24. Krishnan, S., Kiang, J. G., Fisher, C. U., Nambiar, M. P., Nguyen, H. T., Kyttaris, V. C., Chowdhury, B., Rus, V., and Tsokos, G. C. (2005) Increased caspase-3 expression and activity contribute to reduced CD3' expression in systemic lupus erythematosus T cells. J. Immunol. 175, 3417-3423
25. Karni, R., de Stanchina, E., Lowe, S. W., Sinha, R., Mu, D., and Krainer, A. R. (2007) The gene encoding the splicing factor SF2/ASF is a protooncogene. Nat. Struct. Mol. Biol. 14, 185-193
26. Chalfant, C. E., Rathman, K., Pinkerman, R. L., Wood, R. E., Obeid, L. M., Ogretmen, B., and Hannun, Y. A. (2002) De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J. Biol. Chem. 277, 12587-12595
27. Li, X., Wang, J., and Manley, J. L. (2005) Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation. Genes Dev. 19, 2705-2714
28. Dragone, L. L., Shaw, L. A., Myers, M. D., and Weiss, A. (2009) SLAP, a regulator of immunoreceptor ubiquitination, signaling, and trafficking. Immunol. Rev. 232, 218-228
29. Li, D., Gál, I., Vermes, C., Alegre, M. L., Chong, A. S., Chen, L., Shao, Q., Adarichev, V., Xu, X., Koreny, T., Mikecz, K., Finnegan, A., Glant, T. T., and Zhang, J. (2004) Cutting edge: Cbl-b: one of the key molecules tuning CD28-and CTLA-4-mediated T cell costimulation. J. Immunol. 173, 7135-7139
30. Zhang, J. (2004) Ubiquitin ligases in T cell activation and autoimmunity. Clin. Immunol. 111, 234-240
31. Sun, S., Zhang, Z., Sinha, R., Karni, R., and Krainer, A. R. (2010) SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol. 17, 306-312
32. Bronevetsky, Y., and Ansel, K. M. (2013) Regulation of miRNA biogenesis and turnover in the immune system. Immunol. Rev. 253, 304-316
33. Sonkoly, E., Stahle, M., and Pivarcsi, A. (2008) MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol. 18, 131-140
34. Kirkpatrick, D. S., Denison, C., and Gygi, S. P. (2005) Weighing in on ubiquitin: the expanding role of mass-spectrometry-based proteomics. Nat. Cell Biol. 7, 750-757
35. Nambiar, M. P., Enyedy, E. J., Fisher, C. U., Krishnan, S., Warke, V. G., Gilliland, W. R., Oglesby, R. J., and Tsokos, G. C. (2002) Abnormal expression of various molecular forms and distribution of T cell receptor chain in patients with systemic lupus erythematosus. Arthritis Rheum. 46, 163-174
36. Higgs, R., Ní Gabhann, J., Ben Larbi, N., Breen, E. P., Fitzgerald, K. A., and Jefferies, C. A. (2008) The E3 ubiquitin ligase Ro52 negatively regulates IFN production post-pathogen recognition by polyubiquitin-mediated degradation of IRF3. J. Immunol. 181, 1780-1786
37. Feist, E., Dörner, T., Kuckelkorn, U., Schmidtke, G., Micheel, B., Hiepe, F., Burmester, G. R., and Kloetzel, P. M. (1996) Proteasome-type subunit C9 is a primary target of autoantibodies in sera of patients with myositis and systemic lupus erythematosus. J. Exp. Med. 184, 1313-1318