Nuclear factor of activated t cells regulates the expression of interleukin-4 in Th2 cells in an All-or-none fashion

Journal of Biological Chemistry

Volumn 289, Issue 39, 2014, Pages 26752-26761

  Köck, Juliana ^a   Kreher, Stephan ^a   Lehmann, Katrin ^a   Riedel, René ^a   Bardua, Markus ^a   Lischke, Timo ^a   Jargosch, Manja ^a   Haftmann, Claudia ^a   Bendfeldt, Hanna ^a   Hatam, Farahnaz ^a   Mashreghi, Mir Farzin ^a   Baumgrass, Ria ^a   Radbruch, Andreas ^a   Chang, Hyun Dong ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

IMMUNOPATHOLOGY; INTERLEUKIN-4; NUCLEAR FACTOR OF ACTIVATED T-CELLS; NUCLEAR TRANSLOCATIONS;

T-CELLS;

BRG1 PROTEIN; CALCINEURIN; E1A ASSOCIATED P300 PROTEIN; INTERLEUKIN 4; STAT6 PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR C MAF; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; TRANSCRIPTION FACTOR NFATC2; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; CMIP PROTEIN, MOUSE; DNA HELICASE; EP300 PROTEIN, MOUSE; GATA3 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; NFATC2 PROTEIN, MOUSE; NUCLEAR PROTEIN; RELA PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMARCA4 PROTEIN, MOUSE; STAT6 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCUS; GENE TRANSLOCATION; IL4 GENE; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; REGULATOR GENE; T LYMPHOCYTE ACTIVATION; TH2 CELL; ACTIVE TRANSPORT; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL NUCLEUS; CYTOLOGY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL NUCLEUS; DNA HELICASES; E1A-ASSOCIATED P300 PROTEIN; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; RESPONSE ELEMENTS; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS;

EID: 84907572375     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.587865     Document Type: Article

References (35)

1. Zhu, J., Yamane, H., and Paul, W. E. (2010) Differentiation of effector CD4 T cell populations (∗). Annu. Rev. Immunol. 28, 445-489
2. Asnagli, H., Afkarian, M., and Murphy, K. M. (2002) Cutting edge: Identification of an alternative GATA-3 promoter directing tissue-specific gene expression in mouse and human. J. Immunol. 168, 4268-4271
3. Scheinman, E. J., and Avni, O. (2009) Transcriptional regulation of GATA3 in T helper cells by the integrated activities of transcription factors downstream of the interleukin-4 receptor and T cell receptor. J. Biol. Chem. 284, 3037-3048
4. Höfer, T., Nathansen, H., Löhning, M., Radbruch, A., and Heinrich, R. (2002) GATA-3 transcriptional imprinting in Th2 lymphocytes: a mathematical model. Proc. Natl. Acad. Sci. U.S.A. 99, 9364-9368
5. Ouyang, W., Löhning, M., Gao, Z., Assenmacher, M., Ranganath, S., Radbruch, A., and Murphy, K. M. (2000) Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity 12, 27-37
6. Zhu, J., Min, B., Hu-Li, J., Watson, C. J., Grinberg, A., Wang, Q., Killeen, N., Urban, J. F., Jr., Guo, L., and Paul, W. E. (2004) Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 5, 1157-1165
7. Tykocinski, L. O., Hajkova, P., Chang, H. D., Stamm, T., Sözeri, O., Löhning, M., Hu-Li, J., Niesner, U., Kreher, S., Friedrich, B., Pannetier, C., Grütz, G., Walter, J., Paul, W. E., and Radbruch, A. (2005)Acritical control element for interleukin-4 memory expression in T helper lymphocytes. J. Biol. Chem. 280, 28177-28185
8. Hutchins, A. S., Mullen, A. C., Lee, H. W., Sykes, K. J., High, F. A., Hendrich, B. D., Bird, A. P., and Reiner, S. L. (2002) Gene silencing quantitatively controls the function of a developmental trans-activator. Mol. Cell 10, 81-91
9. Agarwal, S., Avni, O., and Rao, A. (2000) Cell-type-restricted binding of the transcription factor NFAT to a distal IL-4 enhancer in vivo. Immunity 12, 643-652
10. Lee, G. R., Fields, P. E., Griffin, T. J., and Flavell, R. A. (2003) Regulation of the Th2 cytokine locus by a locus control region. Immunity 19, 145-153
11. Lee, D. U., and Rao, A. (2004) Molecular analysis of a locus control region in the T helper 2 cytokine gene cluster: a target for STAT6 but not GATA3. Proc. Natl. Acad. Sci. U.S.A. 101, 16010-16015
12. Wurster, A. L., and Pazin, M. J. (2008) BRG1-mediated chromatin remodeling regulates differentiation and gene expression of T helper cells. Mol. Cell Biol. 28, 7274-7285
13. Hosokawa, H., Tanaka, T., Suzuki, Y., Iwamura, C., Ohkubo, S., Endoh, K., Kato, M., Endo, Y., Onodera, A., Tumes, D. J., Kanai, A., Sugano, S., and Nakayama, T. (2013) Functionally distinct Gata3/Chd4 complexes coordinately establish T helper 2 (Th2) cell identity. Proc. Natl. Acad. Sci. U.S.A. 110, 4691-4696
14. Löhning, M., Richter, A., Stamm, T., Hu-Li, J., Assenmacher, M., Paul, W. E., and Radbruch, A. (2003) Establishment of memory for IL-10 expression in developing T helper 2 cells requires repetitive IL-4 costimulation and does not impair proliferation. Proc. Natl. Acad. Sci. U.S.A. 100, 12307-12312
15. Hu-Li, J., Pannetier, C., Guo, L., Löhning, M., Gu, H., Watson, C., Assenmacher, M., Radbruch, A., and Paul, W. E. (2001) Regulation of expression of IL-4 alleles: analysis using a chimeric GFP/IL-4 gene. Immunity 14, 1-11
16. Guo, L., Hu-Li, J., and Paul, W. E. (2005) Probabilistic regulation in TH2 cells accounts for monoallelic expression of IL-4 and IL-13. Immunity 23, 89-99
17. 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
18. Okamura, H., Aramburu, J., García-Rodríguez, C., Viola, J. P., Raghavan, A., Tahiliani, M., Zhang, X., Qin, J., Hogan, P. G., and Rao, A. (2000) Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6, 539-550
19. Chang, H. D., Helbig, C., Tykocinski, L., Kreher, S., Koeck, J., Niesner, U., and Radbruch, A. (2007) Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur. J. Immunol. 37, 807-817
20. Stittrich, A. B., Haftmann, C., Sgouroudis, E., Kühl, A. A., Hegazy, A. N., Panse, I., Riedel, R., Flossdorf, M., Dong, J., Fuhrmann, F., Heinz, G. A., Fang, Z., Li, N., Bissels, U., Hatam, F., Jahn, A., Hammoud, B., Matz, M., Schulze, F. M., Baumgrass, R., Bosio, A., Mollenkopf, H. J., Grün, J., Thiel, A., Chen, W., Höfer, T., Loddenkemper, C., Löhning, M., Chang, H. D., Rajewsky, N., Radbruch, A., and Mashreghi, M. F. (2010) The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nat. Immunol. 11, 1057-1062
21. Trevillyan, J. M., Chiou, X. G., Chen, Y. W., Ballaron, S. J., Sheets, M. P., Smith, M. L., Wiedeman, P. E., Warrior, U., Wilkins, J., Gubbins, E. J., Gagne, G. D., Fagerland, J., Carter, G. W., Luly, J. R., Mollison, K. W., and Djuric, S. W. (2001) Potent inhibition of NFAT activation and T cell cytokine production by novel low molecular weight pyrazole compounds. J. Biol. Chem. 276, 48118-48126
22. Frischbutter, S., Gabriel, C., Bendfeldt, H., Radbruch, A., and Baumgrass, R. (2011) Dephosphorylation of Bcl-10 by calcineurin is essential for canonical NF-κB activation in Th cells. Eur. J. Immunol. 41, 2349-2357
23. Aramburu, J., Yaffe, M. B., López-Rodríguez, C., Cantley, L. C., Hogan, P. G., and Rao, A. (1999) Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285, 2129-2133
24. Wei, G., Wei, L., Zhu, J., Zang, C., Hu-Li, J., Yao, Z., Cui, K., Kanno, Y., Roh, T. Y., Watford, W. T., Schones, D. E., Peng, W., Sun, H. W., Paul, W. E., O'Shea, J. J., and Zhao, K. (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155-167
25. Zheng, W., and Flavell, R. A. (1997) The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89, 587-596
26. Lee, G. R., Fields, P. E., and Flavell, R. A. (2001) Regulation of IL-4 gene expression by distal regulatory elements and GATA-3 at the chromatin level. Immunity 14, 447-459
27. Lee, D. U., Agarwal, S., and Rao, A. (2002) Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 16, 649-660
28. Guo, L., Hu-Li, J., and Paul, W. E. (2004) Probabilistic regulation of IL-4 production in Th2 cells: accessibility at the Il4 locus. Immunity 20, 193-203
29. Rivière, I., Sunshine, M. J., and Littman, D. R. (1998) Regulation of IL-4 expression by activation of individual alleles. Immunity 9, 217-228
30. Salazar, C., and Höfer, T. (2005) Activation of the transcription factor NFAT1: concerted or modular regulation? FEBS Lett. 579, 621-626
31. Mariani, L., Schulz, E. G., Lexberg, M. H., Helmstetter, C., Radbruch, A., Löhning, M., and Höfer, T. (2010) Short-term memory in gene induction reveals the regulatory principle behind stochastic IL-4 expression. Mol. Syst. Biol. 6, 359
32. Frischbutter, S., Schultheis, K., Pätzel, M., Radbruch, A., and Baumgrass, R. (2012) Evaluation of calcineurin/NFAT inhibitor selectivity in primary human Th cells using bar-coding and phospho-flow cytometry. Cytometry A 81, 1005-1011
33. Ogryzko, V. V., Schiltz, R. L., Russanova, V., Howard, B. H., and Nakatani, Y. (1996) The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87, 953-959
34. Kupfer, A., Mosmann, T. R., and Kupfer, H. (1991) Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. U.S.A. 88, 775-779
35. Walmsley, B., Alvarez, F. J., and Fyffe, R. E. (1998) Diversity of structure and function at mammalian central synapses. Trends Neurosci. 21, 81-88