Negative regulation of cytokine gene transcription

FASEB Journal

Volumn 11, Issue 11, 1997, Pages 825-833

  Ye, Jianping ^a   Young, Howard A ^b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

DNA methylation; Nuclear factor; T cell

Indexed keywords

CYTOKINE; DNA BINDING PROTEIN; REPRESSOR PROTEIN;

DNA METHYLATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; REVIEW; T LYMPHOCYTE; TRANSCRIPTION REGULATION;

EID: 0030769182     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.11.11.9285480     Document Type: Review

References (99)

1. Zawel, L., and Reinberg, D. (1995) Common themes in assembly and function of eukaryotic transcription complexes (review). Annu. Rev. Biochem. 64, 533-561
2. Pugh, B. F., and Tjian, R. (1991) Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes & Dev. 5, 1935-1945
3. Pugh, B. F., and Tjian, R. (1990) Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61, 1187-1197
4. Tanese, N., Pugh, B. F., and Tjian, R. (1991) Coactivators for a proline-rich activator purified from the multisubunit human TFIID complex. Genes & Dev. 5, 2212-2124
5. Foulkes, N. S., and Sassone-Corsi, P. (1996) Transcription factor couples to the cAMP-signaling pathway. Biochim. Biophys. Acta 1288, F101-F121
6. Chrivia, J. C., Kwok, R. P., Lamb, N., Hagiwara, M., Montminy, M. R., and Goodman, R. H. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature (London) 365, 855-859
7. Kwok, R. P., Lundblad, J. R., Chrivia, J. C., Richards, J. P., Bachinger, H. P., Brennan, R. G., Roberts, S. G., Green, M. R., and Goodman, R. H. (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature (London) 370, 177
8. Janknecht, R., and Hunter, T. (1996) Transcription. A growing coactivator network. Nature (London) 383, 99-103
9. Lang, R. A., Metcalf, D., Cuthbertson, R. A., Lyons, I., Stanley, E., Kelso, A., Kannourakis, G., Williamson, D. J., Klintworth, G. K., Gonda, T. J., and Dunn, A. R. (1987) Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell 51, 675-686
10. Dent, L. A., Strath, M., Mellor, A. L., and Sanderson, C. J. (1990) Eosinophilia in transgenic mice expressing interleukin 5. J. Exp. Med. 172, 1425-1431
11. Suematsu, S., Matsuda, T., Aozasa, K., Akira, S., Nakano, N., Ohno, S., Miyazaki, J.-I., Yamamura, K.-I., and Hirano, T. (1989) IgG1 plasmacytosis in interleukin 6 transgenic mice. Proc. Natl. Acad. Sci. USA 86, 7547-7551
12. Young, H. A., Klinman, D. M., Reynolds, D. A., Grzegorzewski, K. J., Nu, A., Ward, J. M., Winkler-Pickett, R. T., Ortaldo, J. R., Kenny, J. J., and Komschlies, K. L. (1997) Bone marrow and thymus expression of interferon-γ results in severe B-cell lineage reduction, T-cell lineage alterations, and hematopoietic progenitor deficiencies. Blood 89, 583-595
13. Young, H. A., and Hardy, K. J. (1995) Role of interferon-γ in immune cell regulation. J. Leukoc. Biol. 58, 373-381
14. Young, H. A. (1996) Regulation of interferon-γ gene expression. J. Interferon Cytokine Res. 16, 563-568
15. Chrivia, J. C., Wedrychowicz, T., Young, H. A., and Hardy, K. J. (1990) A model of human cytokine regulation based on transfection of gamma interferon gene fragments directly into isolated peripheral blood T lymphocytes. J. Exp. Med. 172, 661-664
16. Penix, L., Weaver, W. M., Pang, Y., Young, H. A., and Wilson, C. B. (1993) Two essential regulatory elements in the human IFN-y promoter confer activation specific expression in T-cells. J. Exp. Med. 178, 1483-1496
17. Gray, P. W., and Goeddel, D. V. (1987) Molecular biology of interferon-gamma. Lymphokines 13, 151-162
18. Dejkema, R., van der Meide, P. H., Pouwels, P. H., Caspers, M., Dubbeld, M., and Schellekens, H. (1985) Cloning and expression of the chromosomal immune interferon gene of the rat. EMBO J. 4, 761-767
19. Devos, K., Duerinck, F., Van Audenhove, K., and Fiers, W. (1992) Cloning and expression of the canine interferon-gamma gene. J. Inteferon Res. 12, 95-102
20. Young, H. A., Ghosh, P., Ye, J., Lederer, J., Lichtman, A., Gerard, J. R., Penix, L., Wilson, C. B., Melvin, A. J., McGurn, M. E., Lewis, D. B., and Taub, D. D. (1994) Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-gamma gene. J. Immunol. 153, 3603-3610
21. Melvin, A. J., McGurn, M. E., Bort, S. J. Gilbson, C., and Lewis, D. B. (1995) Hypomethylation of the interferon-gamma gene correlates with its expression by primary T-lineage cells. Eur. J. Immunol. 25, 426-430
22. Yang, Y., and Li, Q. L. (1990) Restriction enzyme SnaBI is sensitive to methylation of cytosine within its recognition sequence. Nucl. Acids Res. 18, 3083
23. Penix, L. A. Sweetser, M. T., Weaver, W. M., Hoeffler, J. P., Kerppola, T. K., and Wilson, C. B. (1996) The proximal regulatory element of the interferon-gamma promoter mediates selective expression in T cells. J. Biol. Chem. 271, 31964-31972
24. Nabel, G. J., Gorka, C., and Baltimore, D. (1988) T-cell-specific expression of interleukin 2: evidence for a negative regulatory site. Proc. Natl. Acad. Sci. USA 85, 2934-2938
25. Mathey-Prevot, B., Andrews, N. C., Murphy, H. S., Kreissman, S. G., and Nathan, D. G. (1990) Positive and negative elements regulate human interleukin 3 expression. Proc. Natl. Acad. Sci. USA 87, 5046-5050
26. Li-Weber, M., Eder, A., Krafft-Czepa, H., and Krammer, P. H. (1992) T cell-specific negative regulation of transcription of the human cytokine IL-4. J. Immunol. 148, 1913-1918
27. Ray, A., LaForge, K. S., and Sehgal, P. B. (1990) On the mechanism for efficient repression of the interleukin-6 promoter by glucocorticoids: enhancer, TATA box, and RNA start site occlusion. Mol. Cell. Biol. 10, 5736-5746
28. Santhanam, U., Ray, A., and Sehgal, P. B. (1991) Repression of the interleukin 6 gene promoter by p53 and the retinoblastoma susceptibility gene product. Proc. Natl. Acad. Sci. USA 88, 7605-7609
29. Miyatake, S., Shlomai, J., Arai, K., and Arai, N. (1991) Characterization of the mouse granulocyte-macrophage colony-stimulating factor (GM-CSF) gene promoter: nuclear factors that interact with an element shared by three lymphokine genes-those for GM-CSF, interleukin-4 (IL-4), and IL-5. Mol. Cell. Biol. 11, 5894-5901
30. Ye, J., Zhang, X., and Dong, Z. (1996) Characterization of the human granulocyte-macrophage colony-stimulating gene promoter: an API complex and an Sp1-related complex transactivate the promoter activity that is suppressed by a YY1 complex. Mol. Cell. Biol. 16, 157-167
31. Kuhl, D., de la Fuente, J., Chaturvedi, M., Parimoo, S., Ryals, J., Meyer, F., and Weissmann, C. (1987) Reversible silencing of enhancers by sequences derived from the human IFN-alpha promoter. Cell 50, 1057-1069
32. Nourbakhsh, M., Hoffman, K., and Hauser, H. (1993) Interferon-beta promoters contain a DNA element that acts as a position-independent silencer on the NF-kappa B site. EMBO J. 12, 451-459
33. Ye, J., Ghosh, P., Cippitelli, M., Subleski, J., Hardy, K. J., Ortaldo, J. R., and Young, H. A. (1994) Characterization of a silencer regulatory element in the human interferon-gamma promoter. J. Biol. Chem. 269, 25728-25734
34. Fong, C L., Siddiqui, A. H., and Mark, D. F. (1994) Identification and characterization of a novel repressor site in the human tumor necrosis factor alpha gene. Nucl. Acids Res. 22, 1108-1114
35. Nomiyama, H., Hieshima, K., Hirokawa, K., Hattori, T., Takatsuki, K., and Miura, R. (1993) Characterization of cytokine LD78 gene promoters: positive and negative transcriptional factors bind to a negative regulatory element common to LD78, interleukin-3, and granulocyte-macrophage colony-stimulating factor gene promoters. Mol. Cell. Biol. 13, 2787-2801
36. Shi, Y., Seto, E., Chang, L. S., and Shenk, T. (1991) Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67, 377-388
37. Usheva, A., and Shenk, T. (1994) TATA-binding protein-independent initiation: YY1, TFIIB, and RNA polymerase II direct basal transcription on supercoiled template DNA. Cell 76, 1115-1121
38. Kern, S. E., Kinzler, K. W., Bruskin, A., Jarosz, D., Friedman, P., Prives, C., and Vogelstein, B. (1991) Identification of p53 as a sequence-specific DNA-binding protein. Science 252, 1708-1711
39. Leu, X., Miller, C. W., Koeffler, P. H., and Berk, A. J. (1993) The p53 activation domain binds the TATA box-binding polypeptide in Holo-TFIID, and a neighboring p53 domain inhibits transcription. Mol. Cell. Biol. 13, 3291-3300
40. Thut, C. J., Chen, J. L., Klemm, R., and Tjian, R. (1995) p53 transcriptional activation mediated by coactivators sTAFII40 and TAF1160. Science 267, 100-104
41. Farmer, G., Colgan, J., Nakatani, Y., Manley, J. L., and Prives, C. (1996) Functional interaction between p53, the TATA-binding protein (TBP), and TBP-associated factors in vivo. Mol. Cell. Biol. 16, 4295-4304
42. Seto., E., Usheva, A., Zambetti, G. P., Momand, J., Horikoshi, N., Weinmann, R., Levine, A. J., and Shenk, T. (1992) Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl. Acad. Sci. USA 89, 12028-12032
43. Arya, S. K., Wong-Staal, F., and Gallo, R. C. (1984) Dexamethasone-mediated inhibition of human T cell growth factor and gamma-interferon messenger RNA. J. Immunol. 133, 273-276
44. Van Snick, J. (1990) Interleukin-6: an overview. Ann. Rev. Immunol. 8, 253-278.
45. Tanaka, N., and Taniguchi, T. (1992) Cytokine gene regulation: regulatory cis-elements and DNA binding factors involved in the interferon system. Adv. Immunol. 52, 263-281
46. Miyamoto, M., Fujita, T., Kimura, Y., Maruyama, M., Harada, H., Sudo, Y., Miyata, T., and Taniguchi, T. (1988) Regulation expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell 54, 903-913
47. Harada, H. Fujita, T., Miyamoto, M., Kimura, Y., Maruyama, M., Furia, A., Miyata, T., and Taniguchi, T. (1989) Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 58, 729-739
48. Tanaka, N., Kawakami, T., and Taniguchi, T. (1993) Recognition DNA sequences of interferon regulatory factor 1 (IRF-1) and IRF-2, regulators of cell growth and the interferon system. Mol. Cell. Biol. 13, 4531-4538
49. Matsuyama, T., Kimura, T., Kitagawa, M., Pfeffer, K., Kawakami, T., Watanabe, N., Kindig, T. M., Amakawa, R., Kishihara, K., and Wakeham, A. (1993) Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 75, 83-97
50. Cippitelli, M., Sica, A., Viggiano, V., Ye, J., Ghosh, P., Birrer, M. J., and Young, H. A. (1995) Negative transcriptional regulation of the interferon-gamma promoter by glucocorticoids and dominant negative mutants of c-Jun. J. Biol. Chem. 270, 12548-12556
51. Cippitelli, M., Dorman, L., Ortaldo, J. R., and Young, H. A. (1996) The nuclear factor YY1 suppresses the human gamma interferon promoter through two mechanisms: inhibition of AP1 binding and activation of a silencer element. Mol. Cell. Biol. 16, 4744-4753
52. Nimer, S. D., Morita, E. A., Martis, M. J., Wachsman, W., and Gasson, J. C. (1988) Characterization of the human granulocyte-macrophage colony-stimulating factor promoter region by genetic analysis: correlation with DNase I footprinting. Mol. Cell. Biol. 8, 1979-1984
53. Nimer, S., Fraser, J., Richards, J., Lynch, M., and Gasson, J. (1990) The repeated sequence CATT (A/T) is required for granulocyte-macrophage colony-stimulating factor promoter activity. Mol. Cell. Biol. 10, 6084-6088
54. Lenardo, M. J., Kuang, A., Gifford, A., and Baltimore, D. (1988) NF-kappa B protein purification from bovine spleen: nucleotide stimulation and binding site specificity. Proc. Natl. Acad. Sci. USA 85, 8825-8829
55. Liberman, T. A., and Baltimore, D. (1990) Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol. Cell. Biol. 10, 2327-2334
56. Shimizu, H., Mitomo, K., Watanabe, T., Okamoto, S., and Yamamoto, K. (1990) Involvement of a NF-kappa B-like transcription factor in the activation of the interleukin-6 gene by inflammatory lymphokines. Mol. Cell. Biol. 10, 561-568
57. Mukaida, N., Mahe, Y., and Matsushima, K. (1990) Cooperative interaction of nuclear factor-kappa B-and cis-regulatory enhancer binding protein-like factor binding elements in activating the interleukin-8 gene by pro-inflammatory cytokines. J. Biol. Chem. 265, 21128-21133
58. Kunsch, C., Lang, R. K., Rosen, C. A., and Shannon, M. F. (1994) Synergistic transcriptional activation of the IL-8 gene by NF-kappa B p65 (RelA) and NF-IL-6. J. Immunol. 153, 153-164
59. Casolaro, V., Georas, S. N., Song, Z., Zubkoff, I. D., Abdulkadir, S. A., Thanos, D., and Ono, S. J. (1995) Inhibition of NF-AT-dependent transcription by NF-kappa B: implications for differential gene expression in T helper cell subsets. Proc. Natl. Acad. Sci. USA 92, 11623-11627
60. Pfeuffer, I., Klein-Hessling, S., Heinfling, A., Chuvpilo, S., Escher, C., Brabletz, T., Hentsch, B., Schwarzenbach, H., Matthias, P., and Serfling, E. (1994) Octamer factors exert a dual effect on the IL-2 and 11-4 promoters. J. Immunol. 153, 5572-5585
61. Arany, Z., Sellers, W. R., Livingston, D. M., and Eckner, R. (1994) E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell 77, 799-800
62. Lundblad, J. R., Kwok, R. P., Laurance, M. E., Harter, M. L., and Goodman, R. H. (1995) Adenoviral E1A-associated protein p300 as a functional homologue of the transcriptional co-activator CBP. Nature (London) 374, 85-88
63. Eckner, R., Ewen, M. E., Newsome, D., Gerdes, M., DeCaprio, J. A., Lawrence, J. B., and Livingston, D. M. (1994) Molecular cloning and functional analysis of the adenoyirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes & Dev. 8, 869-884
64. Bannister, A. J., Oehler, T., Wilhelm, D., Angel, P., and Kouzarides, T. (1995) Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11, 2509-2514
65. Bannister, A. J., and Kouzarides, T. (1995) CBP-induced stimulation of c-Fos activity is abrogated by E1A. EMBO J. 14, 4758-4762
66. Lee, J. S., Galvin, K. M., See, R. H., Eckner, R., Livingston, D., Moran, E., and Shi, Y. (1995) Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300. Genes & Dev. 9, 1188-1198
67. Kamei, Y., Xu, L., Heinzel, T., Torchia, J., Kurokawa, R., Gloss, B., Lin, S. C., Heyman, R. A., Rose, D. W., Glass, C. K., and Rosenfeld, M. G. (1996) A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85, 403-414
68. Chakravarti, D., LaMorte, V. J., Nelson, M. C., Nakajima, T., Schulman, I. G., Juguilon, H., Montminy, M., and Evans, R. M. (1996) Role of CBP/P300 in nuclear receptor signaling. Nature (London) 383, 99-103
69. Arias, J., Alberts, A. S., Brindle, P., Claret, F. X., Smeal, T., Karin, M., Feramisco, J., and Montminy, M. (1994) Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature (London) 370, 226-229
70. Parker, D., Ferreri, K., Nakajima, T., LaMorte, V. J., Evans, R., Koerber, S. C., Hoeger, C., and Montminy, M. R. (1996) Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16, 694-703
71. Kee, B. L., Arias, J., and Montminy, M. R. (1996) Adaptor-mediated recruitment of RNA polymerase II to a signal-dependent activator. J. Biol. Chem. 271, 2373-2375
72. Ogryzko, V. V., Schlitz, R. L., Russanova, V., Howard, B. H., and Nakatani, Y. (1996) The transcriptional coactivators p300 and CBP are histone acetyltransferase. Cell 87, 953-959
73. Bannister, A. J., and Kouzarides, T. (1996) The CBP co-activator is a histone acetyltransferase. Nature (London) 384, 641-643
74. Sun, P., and Maurer, R. A. (1995) An inactivating point mutation demonstrates that interaction of cAMP response element binding protein (CREB) with the CREB blinding protein is not sufficient for transcriptional activation. J. Biol. Chem. 270, 7041-7044
75. Yang-Yen, H. F., Chambard, J. C., Sun, Y. L., Smeal, T., Schmidt, T. J., Drouin, J., and Karin, M. (1990) Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62, 1205-1215
76. Scala, R., Rangarajan, P., Kliewer, Ransone, L. J., Bolado, J., Yang, N., Verma, I. M., and Evans, R. M. (1990) Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell 62, 1217-1226
77. Jonat, C., Rahmsdorf, H. J., Park, K. K., Cato, A. C., Gebel, S., Ponta, H., and Herrlich, P. (1990) Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 62, 1189-1204
78. Granelli-Piperno, A., Nolan, P., Inaba, K., and Steinman, R. M. (1990) The effect of immunosuppressive agents on the induction of nuclear factors that bind to sites on the interleukin 2 promoter. J. Exp. Med. 172, 1869-1872
79. Pagliogianni, F., Raptis, A., Ahuja, S. S., Najjar, S. M., and Bournpas, D. T. (1993) Negative transcriptional regulation of human interleukin 2 (IL-2) gene by glucocorticoids through interference with nuclear transcription factors AP-1 and NF-AT. J. Clin. Invest. 91, 1481-1489
80. Cantorna, M. T., Nashold, F. E., Chun, T. Y., and Hayes, C. E. (1996) Vitamin A down-regulation of IFN-gamma synthesis in cloned mouse Th1 lymphocytes depends on the CD28 costimulatory pathway. J. Immunol. 156, 2674-2679
81. Cippitelli, M., Ye, J., Viggiano, V., Sica, A., Ghosh, P., Gulino, A., Santoni, A., and Young, H. A. (1996) Retinoic acid-induced transcriptional modulation of the interferon-γ promoter. J. Biol. Chem. 271, 26783-26793
82. de Grazia, U., Felli, M. P., Vacca, A., Farina, A. R., Maroder, M., Cappabianca, L., Meco, D., Farina, M., Screpanti, I., and Frati, L. (1994) Positive and negative regulation of the composite octamer motif of the interleukin 2 enhancer by AP-1, Oct-2, and retinoic acid receptor. J. Exp. Med. 180, 1485-1497
83. Ray, A., Sassone-Corsi, P. And Sehgal, P. B. (1989) A multiple cytokine-and second messenger-responsive element in the enhancer of the human interleukin-6 gene: Similarities with c-fos gene regulation. Mol. Cell. Biol. 9, 5537-5547
84. Tabibzadeh, S. S., Santhanam, U., Sehgal, P. B., and May, L. T. (1989) Cytokine-induced production of IFN-β2/IL-6 by freshly explanted human endometrial stromal cell modulation by estradiol-17. J. Immunol. 142, 3134-3139
85. Girasole, G., Jilka, R. L., Passen, G., Boswell, S., Boder, G., Williams, D. C., and Manolagas, S. C. (1992) 17 beta-estradiol inhibits interleukin-6 production by bone marrow-derived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens. J. Clin. Invest. 89, 883-891
86. Pottratz, S. T., Bellido, T., Mocharla, H., Crabb, D., and Manolagas, S. C. (1994) 17 beta-Estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J. Clin. Invest. 93, 944-950
87. Ray, A., Prefontaine, K. E., and Ray, P. (1994) Down-modulation of interleukin-6 gene expression by 17 beta-estradiol in the absence of high affinity DNA binding by the estrogen receptor. J. Biol. Chem. 269, 12940-12946
88. Stein, B., and Yang, M. X. (1995) Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol. Cell. Biol. 15, 4971-4979
89. Ray, A., Zhang, D., Siegel, M.D. and Ray, P. (1995) Regulation of interleukin-6 gene expression by steroids. Ann N. Y. Acad. Sci. 762, 79-87
90. Rao, A. (1994) NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today 15, 274-281
91. McCaffrey, P. G., Luo, C., Kerppola, T. K., Jain, J., Badalian, T. M., Ho, A. M., Burgeon, E., Lane, W. S., Lambert, J. N., and Curran, T. (1993) Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262, 750-754
92. Northrop, J. P., Ho, S. N., Chen, L., Thomas, D. J., Timmerman, L. A., Nolan, G. P., Admon, A., and Crabtree, G. R. (1994) NF-AT components define a family of transcription factors targeted in T-cell activation. Nature (London) 369, 497-502
93. McCaffrey, P. G., Perrino, B. A., Soderling, T. R., and Rao, A. (1993) NF-ATp, a T lymphocyte DNA-binding protein that is a target for calcineurin and immunosuppressive drugs. J. Biol. Chem. 268, 3747-3752
94. 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 (London) 365, 352-355
95. Shaw, K. T., Ho, A. M., Raghavan, A., Kim, J., Jain, J., Park, J., Sharma, S., Rao, A., and Hogan, P. G. (1995) Immunosuppressive drugs prevent a rapid dephosphorylation of transcription factor NFAT1 in stimulated immune cells. Proc. Natl. Acad. Sci. USA 92, 11205-11209
96. Wesselborg, S., Fruman, D. A., Sagoo, J. K., Bierer, B. E., and Burakoff, S. J. (1996) Identification of a physical interaction between calcineurin and nuclear factor of activated T cells (NFATp). J. Biol. Chem. 271, 1274-1277
97. Luo, C., Burgeon, E., Carew, J. A., McCaffrey, P. G., Badalian, T. M., Lane, W. S., Hogan, P. G., and Rao, A. (1996) Recombinant NFAT1 (NFATp) is regulated by calcineurin in T cells and mediates transcription of several cytokine genes. Mol. Cell. Biol. 16, 3955-3966
98. Campbell, P. M., Pimm, J., Ramassar, V., and Halloran, P. F. (1996) Identification of a calcium-inducible, cyclosporine sensitive element in the IFN-gamma promoter that is a potential NFAT binding site. Transplantation 61, 933-939
99. Ye, J., Ortaldo, J. R., Conlon, K., Winker-Pickett, R., and Young, H. A. (1995) Cellular and molecular mechanisms of IFN-gamma production induced by IL-2 and IL-12 in a human NK cell line. J. Leukoc. Biol. 58, 225-233