Serine arginine-rich splicing factor 1 (SRSF1) contributes to the transcriptional activation of CD3ζ in human T cells

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Moulton, Vaishali R ^a   Gillooly, Andrew R ^a   Perl, Marcel A ^a   Markopoulou, Anastasia ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ZETA SIGNALING CHAIN; MESSENGER RNA; SERINE ARGININE RICH PROTEIN; SERINE ARGININE RICH SPLICING FACTOR 1; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CD3 ANTIGEN; CD3 ANTIGEN, ZETA CHAIN; LUCIFERASE; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BINDING; SERINE ARGININE RICH SPLICING FACTOR; SMALL INTERFERING RNA; SRSF1 PROTEIN, HUMAN;

ARTICLE; CD3 ZETA SIGNALING CHAIN GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR PATHOLOGY; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; 3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANTAGONISTS AND INHIBITORS; CASE CONTROL STUDY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; JURKAT CELL LINE; METABOLISM; PATHOLOGY; PRIMARY CELL CULTURE; REPORTER GENE; SIGNAL TRANSDUCTION;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; ANTIGENS, CD3; CASE-CONTROL STUDIES; CHROMATIN IMMUNOPRECIPITATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENES, REPORTER; HUMANS; JURKAT CELLS; LUCIFERASES; LUPUS ERYTHEMATOSUS, SYSTEMIC; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; RNA, SMALL INTERFERING; SERINE-ARGININE SPLICING FACTORS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION;

EID: 84940026126     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131073     Document Type: Article

References (34)

1. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011; 365(22):2110-21. Epub 2011/12/02. doi: 10.1056/NEJMra1100359 PMID: 22129255.
2. Moulton VR, Tsokos GC. Abnormalities of T cell signaling in systemic lupus erythematosus. Arthritis Res Ther. 2011; 13(2):207. Epub 2011/04/05. doi: ar3251 [pii] doi: 10.1186/ar3251 PMID: 21457530; PubMed Central PMCID: PMCPMC3132009.
3. Nambiar MP, Enyedy EJ, Warke VG, Krishnan S, Dennis G, Kammer GM, et al. Polymorphisms/mutations of TCR-zeta-chain promoter and 3' untranslated region and selective expression of TCR zetachain with an alternatively spliced 3' untranslated region in patients with systemic lupus erythematosus. Journal of autoimmunity. 2001; 16(2):133-42. Epub 2001/03/15. doi: 10.1006/jaut.2000.0475 S0896-8411(00)90475-X [pii]. PMID: 11247639; PubMed Central PMCID: PMCPMC Journal - In Process.
4. Brundula V, Rivas LJ, Blasini AM, Paris M, Salazar S, Stekman IL, et al. Diminished levels of T cell receptor zeta chains in peripheral blood T lymphocytes from patients with systemic lupus erythematosus. Arthritis and rheumatism. 1999; 42(9):1908-16. Epub 1999/10/08. doi: 10.1002/1529-0131(199909)42:9<1908::AID-ANR17>3.0.CO;2-7 PMID: 10513807; PubMed Central PMCID: PMCPMC Journal - In Process.
5. Perl A. Pathogenic mechanisms in systemic lupus erythematosus. Autoimmunity. 2010; 43(1):1-6. Epub 2009/12/18. doi: 10.3109/08916930903374741 PMID: 20014960; PubMed Central PMCID: PMCPMC Journal - In Process.
6. Liossis SN, Ding XZ, Dennis GJ, Tsokos GC. Altered pattern of TCR/CD3-mediated protein-tyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor zeta chain. The Journal of clinical investigation. 1998; 101(7):1448-57. Epub 1998/04/29. doi: 10.1172/JCI1457 PMID: 9525988; PubMed Central PMCID: PMCPMC508723.
7. Enyedy EJ, Nambiar MP, Liossis SN, Dennis G, Kammer GM, Tsokos GC. Fc epsilon receptor type I gamma chain replaces the deficient T cell receptor zeta chain in T cells of patients with systemic lupus erythematosus. Arthritis and rheumatism. 2001; 44(5):1114-21. PMID: 11352243.
8. Chan AC, Iwashima M, Turck CW, Weiss A. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell. 1992; 71(4):649-62. PMID: 1423621.
9. Krishnan S, Farber DL, Tsokos GC. T cell rewiring in differentiation and disease. J Immunol. 2003; 171(7):3325-31. PMID: 14500623.
10. Nambiar MP, Fisher CU, Warke VG, Krishnan S, Mitchell JP, Delaney N, et al. Reconstitution of deficient T cell receptor zeta chain restores T cell signaling and augments T cell receptor/CD3-induced interleukin-2 production in patients with systemic lupus erythematosus. Arthritis and rheumatism. 2003; 48(7):1948-55. Epub 2003/07/09. doi: 10.1002/art.11072 PMID: 12847689; PubMed Central PMCID: PMCPMC Journal - In Process.
11. Chowdhury B, Tsokos CG, Krishnan S, Robertson J, Fisher CU, Warke RG, et al. Decreased stability and translation of T cell receptor zeta mRNA with an alternatively spliced 3'-untranslated region contribute to zeta chain down-regulation in patients with systemic lupus erythematosus. The Journal of biological chemistry. 2005; 280(19):18959-66. Epub 2005/03/04. doi: M501048200 [pii] doi: 10.1074/jbc. M501048200 PMID: 15743765; PubMed Central PMCID: PMCPMC Journal - In Process.
12. Moulton VR, Kyttaris VC, Juang YT, Chowdhury B, Tsokos GC. The RNA-stabilizing protein HuR regulates the expression of zeta chain of the human T cell receptor-associated CD3 complex. The Journal of biological chemistry. 2008; 283(29):20037-44. Epub 2008/05/29. doi: M710434200 [pii] doi: 10.1074/jbc.M710434200 PMID: 18505733; PubMed Central PMCID: PMCPMC2459291.
13. Moulton VR, Tsokos GC. Alternative splicing factor/splicing factor 2 regulates the expression of the zeta subunit of the human T cell receptor-associated CD3 complex. The Journal of biological chemistry. 2010; 285(17):12490-6. Epub 2010/02/02. doi: M109.091660 [pii] doi: 10.1074/jbc.M109.091660 PMID: 20118245; PubMed Central PMCID: PMCPMC2857141.
14. Moulton VR, Grammatikos AP, Fitzgerald LM, Tsokos GC. Splicing factor SF2/ASF rescues IL-2 production in T cells from systemic lupus erythematosus patients by activating IL-2 transcription. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(5):1845-50. Epub 2013/01/16. doi: 10.1073/pnas.1214207110 PMID: 23319613; PubMed Central PMCID: PMCPMC3562779.
15. Caceres JF, Screaton GR, Krainer AR. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes & development. 1998; 12(1):55-66. Epub 1998/02/21. PMID: 9420331; PubMed Central PMCID: PMCPMC316398.
16. Black DL. Mechanisms of alternative pre-messenger RNA splicing. Annual review of biochemistry. 2003; 72:291-336. PMID: 12626338.
17. Lemaire R, Prasad J, Kashima T, Gustafson J, Manley JL, Lafyatis R. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes & development. 2002; 16(5):594-607. Epub 2002/03/06. doi: 10.1101/gad.939502 PMID: 11877379; PubMed Central PMCID: PMCPMC155348.
18. Michlewski G, Sanford JR, Caceres JF. The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Molecular cell. 2008; 30(2):179-89. Epub 2008/04/29. doi: S1097-2765(08)00237-2 [pii] doi: 10.1016/j.molcel.2008.03.013 PMID: 18439897; PubMed Central PMCID: PMCPMC Journal - In Process.
19. Lin S, Coutinho-Mansfield G, Wang D, Pandit S, Fu XD. The splicing factor SC35 has an active role in transcriptional elongation. Nature structural & molecular biology. 2008; 15(8):819-26. Epub 2008/07/22. doi: 10.1038/nsmb.1461 PMID: 18641664; PubMed Central PMCID: PMCPMC2574591.
20. Ji X, Zhou Y, Pandit S, Huang J, Li H, Lin CY, et al. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell. 2013; 153(4):855-68. Epub 2013/05/15. doi: 10.1016/j.cell.2013.04.028 PMID: 23663783.
21. Mo S, Ji X, Fu XD. Unique role of SRSF2 in transcription activation and diverse functions of the SR and hnRNP proteins in gene expression regulation. Transcription. 2013; 4(5). Epub 2014/01/11. PMID: 24406341.
22. Chalfant CE, Rathman K, Pinkerman RL, Wood RE, Obeid LM, Ogretmen B, et al. De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. The Journal of biological chemistry. 2002; 277(15):12587-95. Epub 2002/01/22. doi: 10.1074/jbc.M112010200 M112010200 [pii]. PMID: 11801602; PubMed Central PMCID: PMCPMC Journal - In Process.
23. Lemaire R, Winne A, Sarkissian M, Lafyatis R. SF2 and SRp55 regulation of CD45 exon 4 skipping during T cell activation. European journal of immunology. 1999; 29(3):823-37. Epub 1999/03/26. doi: 10.1002/(SICI)1521-4141(199903)29:03<823::AID-IMMU823>3.0.CO;2-C [pii]. PMID: 10092085; PubMed Central PMCID: PMCPMC Journal - In Process.
24. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis and rheumatism. 1982; 25(11):1271-7. PMID: 7138600.
25. Rellahan BL, Jensen JP, Weissman AM. Transcriptional regulation of the T cell antigen receptor zeta subunit: identification of a tissue-restricted promoter. The Journal of experimental medicine. 1994; 180(4):1529-34. Epub 1994/10/01. PMID: 7931084; PubMed Central PMCID: PMC2191675.
26. Rellahan BL, Jensen JP, Howcroft TK, Singer DS, Bonvini E, Weissman AM. Elf-1 regulates basal expression from the T cell antigen receptor zeta-chain gene promoter. J Immunol. 1998; 160(6):2794-801. PMID: 9510181.
27. Kalashnikova AA, Winkler DD, McBryant SJ, Henderson RK, Herman JA, DeLuca JG, et al. Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus. Nucleic acids research. 2013; 41(7):4026-35. Epub 2013/02/26. doi: 10.1093/nar/gkt104 PMID: 23435226; PubMed Central PMCID: PMC3627596.
28. Loomis RJ, Naoe Y, Parker JB, Savic V, Bozovsky MR, Macfarlan T, et al. Chromatin binding of SRp20 and ASF/SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation. Molecular cell. 2009; 33(4):450-61. Epub 2009/03/03. doi: 10.1016/j.molcel.2009.02.003 PMID: 19250906; PubMed Central PMCID: PMC2667802.
29. Juang YT, Tenbrock K, Nambiar MP, Gourley MF, Tsokos GC. Defective production of functional 98-kDa form of Elf-1 is responsible for the decreased expression of TCR zeta-chain in patients with systemic lupus erythematosus. J Immunol. 2002; 169(10):6048-55. PMID: 12421992.
30. Tenbrock K, Kyttaris VC, Ahlmann M, Ehrchen JM, Tolnay M, Melkonyan H, et al. The cyclic AMP response element modulator regulates transcription of the TCR zeta-chain. J Immunol. 2005; 175(9):5975-80. PMID: 16237091.
31. Krishnan S, Kiang JG, Fisher CU, Nambiar MP, Nguyen HT, Kyttaris VC, et al. Increased caspase-3 expression and activity contribute to reduced CD3zeta expression in systemic lupus erythematosus T cells. J Immunol. 2005; 175(5):3417-23. Epub 2005/08/24. doi: 175/5/3417 [pii]. PMID: 16116236; PubMed Central PMCID: PMCPMC Journal - In Process.
32. Fernandez DR, Telarico T, Bonilla E, Li Q, Banerjee S, Middleton FA, et al. Activation of mammalian target of rapamycin controls the loss of TCRzeta in lupus T cells through HRES-1/Rab4-regulated lysosomal degradation. J Immunol. 2009; 182(4):2063-73. Epub 2009/02/10. doi: 182/4/2063 [pii] doi: 10.4049/jimmunol.0803600 PMID: 19201859; PubMed Central PMCID: PMCPMC2676112.
33. Nambiar MP, Enyedy EJ, Fisher CU, Krishnan S, Warke VG, Gilliland WR, et al. Abnormal expression of various molecular forms and distribution of T cell receptor zeta chain in patients with systemic lupus erythematosus. Arthritis and rheumatism. 2002; 46(1):163-74. Epub 2002/01/31. doi: 10.1002/1529-0131(200201)46:1<163::AID-ART10065>3.0.CO;2-J PMID: 11817588; PubMed Central PMCID: PMCPMC Journal - In Process.
34. Moulton VR, Gillooly AR, Tsokos GC. Ubiquitination regulates expression of the serine/arginine-rich splicing factor 1 (SRSF1) in normal and systemic lupus erythematosus (SLE) T cells. The Journal of biological chemistry. 2014; 289(7):4126-34. Epub 2013/12/26. doi: 10.1074/jbc.M113.518662 PMID: 24368769; PubMed Central PMCID: PMC3924278.