Stable IL-2 decision making by endogenous c-Fos amounts in peripheral memory T-helper cells

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18386-18397

  Bendfeldt, Hanna ^a   Benary, Manuela ^b   Scheel, Tobias ^a   Frischbutter, Stefan ^a   Abajyan, Anna ^a   Radbruch, Andreas ^a,c   Herzel, Hanspeter ^a   Baumgrass, Ria ^a  

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE EXPRESSION; CYTOKINES; EXPRESSION LEVELS; HUMAN MEMORY; IMMUNE RESPONSE; PHYSIOLOGICAL DIFFERENCES; SINGLE CELLS; TH CELL; TRANSCRIPTION FACTOR EXPRESSION;

CELLS; FLOW CYTOMETRY; IMMUNOLOGY; TRANSCRIPTION FACTORS;

CYTOLOGY;

INTERLEUKIN 2; PROTEIN C FOS; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC2; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HELPER CELL; HUMAN; HUMAN CELL; MEMORY T LYMPHOCYTE; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; QUANTITATIVE STUDY; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2; NFATC TRANSCRIPTION FACTORS; PROTO-ONCOGENE PROTEINS C-FOS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84861541291     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.358853     Document Type: Article

References (44)

1. Cho, J. H., Boyman, O., Kim, H. O., Hahm, B., Rubinstein, M. P., Ramsey, C., Kim, D. M., Surh, C. D., and Sprent, J. (2007) An intense form of homeostatic proliferation of naive CD8+ cells driven by IL-2. J. Exp. Med. 204, 1787-1801 (Pubitemid 47236317)
2. Dooms, H., Kahn, E., Knoechel, B., and Abbas, A. K. (2004) IL-2 induces a competitive survival advantage in T lymphocytes. J. Immunol. 172, 5973-5979 (Pubitemid 38621197)
3. Dooms, H., Wolslegel, K., Lin, P., and Abbas, A. K. (2007) Interleukin-2 enhances CD4+ T cell memory by promoting the generation of IL-7R alpha-expressing cells. J. Exp. Med. 204, 547-557 (Pubitemid 46457078)
4. Liao, W., Schones, D. E., Oh, J., Cui, Y., Cui, K., Roh, T. Y., Zhao, K., and Leonard, W. J. (2008) Priming for T helper type 2 differentiation by interleukin 2-mediated induction of interleukin 4 receptor-chain expression. Nat. Immunol. 9, 1288-1296
5. Laurence, A., Tato, C. M., Davidson, T. S., Kanno, Y., Chen, Z., Yao, Z., Blank, R. B., Meylan, F., Siegel, R., Hennighausen, L., Shevach, E. M., and O'Shea J, J. (2007) Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26, 371-381 (Pubitemid 46413906)
6. Malek, T. R., Yu, A., Vincek, V., Scibelli, P., and Kong, L. (2002) CD4 regulatory T cells prevent lethal autoimmunity in IL-2Rβ-deficient mice. Implications for the nonredundant function of IL-2. Immunity 17, 167-178 (Pubitemid 35245959)
7. Suzuki, H., Kündig, T. M., Furlonger, C., Wakeham, A., Timms, E., Matsuyama, T., Schmits, R., Simard, J. J., Ohashi, P. S., and Griesser, H. (1995) Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor β. Science 268, 1472-1476
8. Durand, D. B., Shaw, J. P., Bush, M. R., Replogle, R. E., Belagaje, R., and Crabtree, G. R. (1988) Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell Biol. 8, 1715-1724
9. Rooney, J. W., Sun, Y. L., Glimcher, L. H., and Hoey, T. (1995) Novel NFAT sites that mediate activation of the interleukin-2 promoter in response to T-cell receptor stimulation. Mol. Cell Biol. 15, 6299-6310
10. Ullman, K. S., Flanagan, W. M., Edwards, C. A., and Crabtree, G. R. (1991) Activation of early gene expression in T lymphocytes by Oct-1 and an inducible protein, OAP40. Science 254, 558-562 (Pubitemid 21917372)
11. Garrity, P. A., Chen, D., Rothenberg, E. V., and Wold, B. J. (1994) Interleukin-2 transcription is regulated in vivo at the level of coordinated binding of both constitutive and regulated factors. Mol. Cell Biol. 14, 2159-2169 (Pubitemid 24074613)
12. Jain, J., Valge-Archer, V. E., Sinskey, A. J., and Rao, A. (1992) The AP-1 site at -150 bp, but not the NF-κB site, is likely to represent the major target of protein kinase C in the interleukin 2 promoter. J. Exp. Med. 175, 853-862
13. Hughes, C. C., and Pober, J. S. (1996) Transcriptional regulation of the interleukin-2 gene in normal human peripheral blood T cells. Convergence of costimulatory signals and differences from transformed T cells. J. Biol. Chem. 271, 5369-5377
14. Jain, J., Nalefski, E. A., McCaffrey, P. G., Johnson, R. S., Spiegelman, B. M., Papaioannou, V., and Rao, A. (1994) Normal peripheral T-cell function in c-Fos-deficient mice. Mol. Cell Biol. 14, 1566-1574 (Pubitemid 24074552)
15. Xanthoudakis, S., Viola, J. P., Shaw, K. T., Luo, C., Wallace, J. D., Bozza, P. T., Luk, D. C., Curran, T., and Rao, A. (1996) An enhanced immune response in mice lacking the transcription factor NFAT1. Science 272, 892-895
16. Doi, T. S., Takahashi, T., Taguchi, O., Azuma, T., and Obata, Y. (1997) NF-κB RelA-deficient lymphocytes. Normal development of T cells and B cells, impaired production of IgA and IgG1 and reduced proliferative responses. J. Exp. Med. 185, 953-961 (Pubitemid 27119879)
17. Ochi, Y., Koizumi, T., Kobayashi, S., Phuchareon, J., Hatano, M., Takada, M., Tomita, Y., and Tokuhisa, T. (1994) Analysis of IL-2 gene regulation in c-Fos transgenic mice. Evidence for an enhancement of IL-2 expression in splenic T cells stimulated via TCR/CD3 complex. J. Immunol. 153, 3485-3490 (Pubitemid 24313851)
18. Peng, S. L., Gerth, A. J., Ranger, A. M., and Glimcher, L. H. (2001) NFATc1 and NFATc2 together control both T and B cell activation and differentiation. Immunity 14, 13-20 (Pubitemid 32144683)
19. Yui, M. A., Sharp, L. L., Havran, W. L., and Rothenberg, E. V. (2004) Preferential activation of an IL-2 regulatory sequence transgene in TCRγδand NKT cells. Subset-specific differences in IL-2 regulation. J. Immunol. 172, 4691-4699 (Pubitemid 38456389)
20. Feinerman, O., Veiga, J., Dorfman, J. R., Germain, R. N., and Altan-Bonnet, G. (2008) Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 321, 1081-1084
21. Podtschaske, M., Benary, U., Zwinger, S., Höfer, T., Radbruch, A., and Baumgrass, R. (2007) Digital NFATc2 activation per cell transforms graded T cell receptor activation into an all-or-none IL-2 expression. PLoS One 2, e935
22. Bintu, L., Buchler, N. E., Garcia, H. G., Gerland, U., Hwa, T., Kondev, J., and Phillips, R. (2005) Transcriptional regulation by the numbers. Models. Curr. Opin. Genet. Dev. 15, 116-124
23. Hori, S., Nomura, T., and Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061 (Pubitemid 36222930)
24. Hickman, S. P., Yang, J., Thomas, R. M., Wells, A. D., and Turka, L. A. (2006) Defective activation of protein kinase C and Ras-ERK pathways limits IL-2 production and proliferation by CD4+CD25+ regulatory T cells. J. Immunol. 177, 2186-2194 (Pubitemid 44200977)
25. Carson, B. D., and Ziegler, S. F. (2007) ImpairedTcell receptor signaling in Foxp3+ CD4 T cells. Ann. N.Y. Acad. Sci. 1103, 167-178 (Pubitemid 46791122)
26. Buchler, N. E., Gerland, U., and Hwa, T. (2003) On schemes of combinatorial transcription logic. Proc. Natl. Acad. Sci. U.S.A. 100, 5136-5141 (Pubitemid 36542671)
27. Chu, D., Zabet, N. R., and Mitavskiy, B. (2009) Models of transcription factor binding. Sensitivity of activation functions to model assumptions. J. Theor Biol. 257, 419-429
28. Bryan, R. G., Li, Y., Lai, J. H., Van, M., Rice, N. R., Rich, R. R., and Tan, T. H. (1994) Effect of CD28 signal transduction on c-Rel in human peripheral blood T cells. Mol. Cell Biol. 14, 7933-7942 (Pubitemid 24373542)
29. Jain, J., McCaffrey, P. G., Miner, Z., Kerppola, T. K., Lambert, J. N., Verdine, G. L., Curran, T., and Rao, A. (1993) The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365, 352-355 (Pubitemid 23288978)
30. Rothenberg, E. V., and Ward, S. B. (1996) A dynamic assembly of diverse transcription factors integrates activation and cell-type information for interleukin 2 gene regulation. Proc. Natl. Acad. Sci. U.S.A. 93, 9358 -9365
31. Fiering, S., Northrop, J. P., Nolan, G. P., Mattila, P. S., Crabtree, G. R., and Herzenberg, L. A. (1990) Single cell assay of a transcription factor reveals a threshold in transcription activated by signals emanating from the T-cell antigen receptor. Genes Dev. 4, 1823-1834
32. Pirone, J. R., and Elston, T. C. (2004) Fluctuations in transcription factor binding can explain the graded and binary responses observed in inducible gene expression. J. Theor. Biol. 226, 111-121
33. Dienz, O., Eaton, S. M., Krahl, T. J., Diehl, S., Charland, C., Dodge, J., Swain, S. L., Budd, R. C., Haynes, L., and Rincon, M. (2007) Accumulation of NFAT mediates IL-2 expression in memory, but not naive, CD4+ T cells. Proc. Natl. Acad. Sci. U.S.A. 104, 7175-7180 (Pubitemid 47186028)
34. Jain, J., Loh, C., and Rao, A. (1995) Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7, 333-342
35. Petrak, D., Memon, S. A., Birrer, M. J., Ashwell, J. D., and Zacharchuk, C. M. (1994) Dominant negative mutant of c-Jun inhibits NF-AT transcriptional activity and prevents IL-2 gene transcription. J. Immunol. 153, 2046-2051 (Pubitemid 24256675)
36. Serfling, E., Avots, A., and Neumann, M. (1995) The architecture of the interleukin-2 promoter. A reflection of T lymphocyte activation. Biochim. Biophys. Acta 1263, 181-200
37. Villarino, A. V., Tato, C. M., Stumhofer, J. S., Yao, Z., Cui, Y. K., Hen nighausen, L., O'Shea, J. J., and Hunter, C. A. (2007) Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J. Exp. Med. 204, 65-71 (Pubitemid 46148757)
38. Kang, S. M., Tran, A. C., Grilli, M., and Lenardo, M. J. (1992) NF-κB subunit regulation in nontransformed CD4+T lymphocytes. Science 256, 1452-1456
39. Hwang, E. S., Hong, J. H., and Glimcher, L. H. (2005) IL-2 production in developing Th1 cells is regulated by heterodimerization of RelA and T-bet and requires T-bet serine residue 508. J. Exp. Med. 202, 1289-1300
40. Wakabayashi, Y., Tamiya, T., Takada, I., Fukaya, T., Sugiyama, Y., Inoue, N., Kimura, A., Morita, R., Kashiwagi, I., Takimoto, T., Nomura, M., and Yoshimura, A. (2011) Histone 3 lysine 9 (H3K9) methyltransferase recruitment to the interleukin-2 (IL-2) promoter is a mechanism of suppression of IL-2 transcription by the transforming growth factor-β-Smad pathway. J. Biol. Chem. 286, 35456-35465
41. Wong, W. F., Kurokawa, M., Satake, M., and Kohu, K. (2011) Downregulation of Runx1 expression by TCR signal involves an autoregulatory mechanism and contributes to IL-2 production. J. Biol. Chem. 286, 11110-11118
42. Ohori, M. (2008) ERK inhibitors as a potential new therapy for rheumatoid arthritis. Drug News Perspect. 21, 245-250
43. Koreth, J., Matsuoka, K., Kim, H. T., McDonough, S. M., Bindra, B., Alyea, E. P., 3rd, Armand, P., Cutler, C., Ho, V. T., Treister, N. S., Bienfang, D. C., Prasad, S., Tzachanis, D., Joyce, R. M., Avigan, D. E., Antin, J. H., Ritz, J., and Soiffer, R. J. (2011) Interleukin-2 and regulatory T cells in graft-versus- host disease. N. Engl. J. Med. 365, 2055-2066
44. Saadoun, D., Rosenzwajg, M., Joly, F., Six, A., Carrat, F., Thibault, V., Sene, D., Cacoub, P., and Klatzmann, D. (2011) Regulatory T-cell responses to low-dose interleukin-2 in HCV-induced vasculitis. N. Engl. J. Med. 365, 2067-2077