Engagement of T-cell antigen receptor and CD4/CD8 co-receptors induces prolonged STAT activation through autocrine/paracrine stimulation in human primary T cells

Biochemical and Biophysical Research Communications

Volumn 426, Issue 2, 2012, Pages 242-246

  Chueh, Fu Yu ^a   Yu, Chao Lan ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Cytokine; Lck; Signal transducer and activator of transcription; Suppressor of cytokine signaling; T cell antigen receptor

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; PROTEIN SH2; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; T LYMPHOCYTE RECEPTOR;

ARTICLE; AUTOCRINE EFFECT; CELL STIMULATION; CONTROLLED STUDY; CROSS LINKING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEUKEMIA CELL LINE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANTIGENS, CD4; ANTIGENS, CD8; AUTOCRINE COMMUNICATION; GENE EXPRESSION; HUMANS; JURKAT CELLS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); PARACRINE COMMUNICATION; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; STAT TRANSCRIPTION FACTORS; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES; TYROSINE;

EID: 84866430987     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.08.074     Document Type: Article

References (35)

1. Smith-Garvin J.E., Koretzky G.A., Jordan M.S. T cell activation. Annu. Rev. Immunol. 2009, 27:591-619.
2. Fooksman D.R., Vardhana S., Vasiliver-Shamis G., Liese J., Blair D.A., Waite J., Sacristan C., Victora G.D., Zanin-Zhorov A., Dustin M.L. Functional anatomy of T cell activation and synapse formation. Annu. Rev. Immunol. 2010, 28:79-105.
3. Bierer B.E., Sleckman B.P., Ratnofsky S.E., Burakoff S.J. The biologic roles of CD2, CD4, and CD8 in T-cell activation. Annu. Rev. Immunol. 1989, 7:579-599.
4. Salmond R.J., Filby A., Qureshi I., Caserta S., Zamoyska R. T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol. Rev. 2009, 228:9-22.
5. Chu D.H., Morita C.T., Weiss A. The Syk family of protein tyrosine kinases in T-cell activation and development. Immunol. Rev. 1998, 165:167-180.
6. Nel A.E., Slaughter N. T-cell activation through the antigen receptor. Part 2: role of signaling cascades in T-cell differentiation, energy, immune senescence, and development of immunotherapy. J. Allergy Clin. Immunol. 2002, 109:901-915.
7. Moriggl R., Topham D.J., Teglund S., Sexl V., McKay C., Wang D., Hoffmeyer A., van Deursen J., Sangster M.Y., Bunting K.D., Grosveld G.C., Ihle J.N. STAT5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 1999, 10:249-259.
8. Koretzky G.A., Myung P.S. Positive and negative regulation of T cell activation by adaptor proteins. Nat. Rev. Immunol. 2001, 1:95-107.
9. Palmer D.C., Restifo N.P. Suppressors of cytokine signaling (SOCS) in T cell differentiation, maturation, and function. Trend. Immunol. 2009, 30:592-602.
10. Yoshimura A., Ohkubo T., Kiguchi T., Jenkins N.A., Gilbert D.J., Copeland N.G., Hara T., Miyajima A. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J. 1995, 14:2816-2826.
11. Fujimoto M., Naka T., Nakagawa R., Kawazoe Y., Morita Y., Tateishi A., Okumura K., Narazaki M., Kishimoto T. Defective thymocyte development and perturbed homeostasis of T cells in STAT-induced STAT inhibitor-1/suppressors of cytokine signaling-1 transgenic mice. J. Immunol. 2000, 165:1799-1806.
12. Cornish A.L., Davey G.M., Metcalf D., Purton J.F., Corbin J.E., Greenhalgh C.J., Darwiche R., Wu L., Nicola N.A., Godfrey D.I., Heath W.R., Hilton D.J., Alexander W.S., Starr R. Suppressor of cytokine signaling-1 has IFN-gamma-independent actions in T cell homeostasis. J. Immunol. 2003, 170:878-886.
13. Trop S., de Sepulveda P., Zuniga-Pflucker J.C., Rottapel R. Overexpression of suppressor of cytokine signaling-1 impairs pre-T cell receptor-induced proliferation but not differentiation of immature thymocytes. Blood 2001, 97:2269-2277.
14. Fletcher J., Starr R. The role of suppressors of cytokine signalling in thymopoiesis and T cell activation. Int. J. Biochem. Cell Biol. 2005, 37:1774-1786.
15. Okugawa S., Yanagimoto S., Tsukada K., Kitazawa T., Koike K., Kimura S., Nagase H., Hirai K., Ota Y. Bacterial flagellin inhibits T cell receptor-mediated activation of T cells by inducing suppressor of cytokine signalling-1 (SOCS-1). Cell. Microbiol. 2006, 8:1571-1580.
16. Matsuda T., Yamamoto T., Kishi H., Yoshimura A., Muraguchi A. SOCS-1 can suppress CD3zeta- and Syk-mediated NF-AT activation in a non-lymphoid cell line. FEBS Lett. 2000, 472:235-240.
17. Banerjee A., Banks A.S., Nawijn M.C., Chen X.P., Rothman P.B. Cutting edge: suppressor of cytokine signaling 3 inhibits activation of NFATp. J. Immunol. 2002, 168:4277-4281.
18. Welte T., Leitenberg D., Dittel B.N., Al-Ramadi B.K., Xie B., Chin Y.E., Janeway C.A., Bothwell A.L., Bottomly K., Fu X.Y. STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science 1999, 283:222-225.
19. Yu C.-L., Jove R., Burakoff S.J. Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase. J. Immunol. 1997, 159:5206-5210.
20. Chueh F.-Y., Leong K.-F., Yu C.-L. Mitochondrial translocation of signal transducer and activator of transcription 5 (STAT5) in leukemic T cells and cytokine-stimulated cells. Biochem. Biophys. Res. Commun. 2010, 402:778-783.
21. Cooper J.C., Shi M., Chueh F.-Y., Venkitachalam S., Yu C.-L. Enforced SOCS1 and SOCS3 expression attenuates Lck-mediated cellular transformation. Int. J. Oncol. 2010, 36:1201-1208.
22. Cooper J.C., Boustead J.N., Yu C.-L. Characterization of STAT5B phosphorylation correlating with expression of cytokine-inducible SH2-containing protein (CIS). Cell. Signal. 2006, 18:851-860.
23. Venkitachalam S., Chueh F.-Y., Leong K.-F., Pabich S., Yu C.-L. Suppressor of cytokine signaling 1 interacts with oncogenic lymphocyte-specific protein tyrosine kinase. Oncol. Rep. 2011, 25:677-683.
24. Shi M., Cooper J.C., Yu C.-L. A constitutively active Lck kinase promotes cell proliferation and resistance to apoptosis through signal transducer and activator of transcription 5b activation. Mol. Cancer Res. 2006, 4:39-45.
25. Ravichandran K.S., Pratt J.C., Sawasdikosol S., Irie H.Y., Burakoff S.J. Co-receptors and adapter proteins in T cell signaling. Anna. NY Acad. Sci. 1995, 766:117-133.
26. Moriggl R., Sexl V., Piekorz R., Topham D., Ihle J.N. STAT5 activation is uniquely associated with cytokine signaling in peripheral T cells. Immunity 1999, 11:225-230.
27. Bierer B.E., Hollander G., Fruman D., Burakoff S.J. Cyclosporin A and FK506: molecular mechanisms of immunosuppression and probes for transplantation biology. Curr. Opin. Immunol. 1993, 5:763-773.
28. Girdlestone J., Wing M. Autocrine activation by interferon-gamma of STAT factors following T cell activation. Eur. J. Immunol. 1996, 26:704-709.
29. Henttinen T., Levy D.E., Silvennoinen O., Hurme M. Activation of the signal transducer and transcription (STAT) signaling pathway in a primary T cell response. Critical role for IL-6. J. Immunol. 1995, 155:4582-4587.
30. Chen X.P., Losman J.A., Rothman P. SOCS proteins, regulators of intracellular signaling. Immunity 2000, 13:287-290.
31. Yu C.-L., Jin Y.J., Burakoff S.J. Cytosolic tyrosine dephosphorylation of STAT5. Potential role of SHP-2 in STAT5 regulation. J. Biol. Chem. 2000, 275:599-604.
32. Yoshimura A. Negative regulation of cytokine signaling. Clin. Rev. Allergy Immunol. 2005, 28:205-220.
33. O'Sullivan L.A., Liongue C., Lewis R.S., Stephenson S.E.M., Ward A.C. Cytokine receptor signaling through the Jak-STAT-SOCS pathway in disease. Mol. Immunol. 2007, 44:2497-2506.
34. Yu C.-R., Mahdi R.M., Ebong S., Vistica B.P., Gery I., Egwuagu C.E. Suppressor of cytokine signaling 3 regulates proliferation and activation of T helper cells. J. Biol. Chem. 2003, 278:29752-29759.
35. Li S., Chen S., Xu X., Sundstedt A., Paulsson K.M., Anderson P., Karlsson S., Sjogrenn H.-O., Wang P. Cytokine-induced Src homology 2 protein (CIS) promotes T cell receptor-mediated proliferation and prolongs survival of activated T cells. J. Exp. Med. 2000, 191:985-994.