Reciprocal Modulatory Interaction between Human Immunodeficiency Virus Type 1 Tat and Transcription Factor NFAT1

REFERENCES

• Alcami, J., T. Lain de Lera, L. Folgueira, M.-A. Pedraza, J.-M. Jacque, F. Bachelerie, A. R. Noriega, R. T. Hay, D. Harrich, R. B. Gaynor, J.-L. Virelizier, and J. Arenzana-Seisdedos 1995. Absolute dependence on κB responsive elements for initiation and Tat-mediated amplification of HIV transcription in blood CD4+ T lymphocytes. EMBO J. 14:1552–1560.
   PubMed Web of Science ®Google Scholar
• Ambrosino, C., M. R. Ruocco, X. Chen, M. Mallardo, F. Baudi, S. Trematerra, I. Quinto, S. Venuta, and J. Scala 1997. HIV-1 Tat induces the expression of the interleukin-6 (IL6) gene by binding to the IL6 leader RNA and by interacting with CAAT enhancer-binding protein beta (NF-IL6) transcription factors. J. Biol. Chem. 272:14883–14892.
   PubMed Web of Science ®Google Scholar
• Aramburu, J., L. Azzoni, A. Rao, and J. Perussia 1995. Activation and expression of the nuclear factor of activated T cells, NFATp and NFATc, in human natural killer cells: regulation upon CD16 ligand binding. J. Exp. Med. 182:801–810.
   PubMedGoogle Scholar
• Berkhout, B., and J. Jeang 1992. Functional roles for the TATA promoter and enhancers in basal and Tat-induced expression of the human immunodeficiency type 1 long terminal repeat. J. Virol. 66:139–149.
   PubMed Web of Science ®Google Scholar
• Blau, J., H. Xiao, S. McCracken, P. O’Hare, J. Greenblatt, and J. Bentley 1996. Three functional classes of transcriptional activation domains. Mol. Cell. Biol. 16:2044–2055.
   PubMed Web of Science ®Google Scholar
• Braaten, D., C. Aberham, E. K. Franke, L. Yin, W. Phares, and J. Luban 1996. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70:5170–5176.
   PubMed Web of Science ®Google Scholar
• Buonaguro, L., G. Barillari, H. K. Chang, C. A. Bohan, V. Kao, R. Morgan, R. C. Gallo, and J. Ensoli 1992. Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines. J. Virol. 66:7159–7167.
   PubMed Web of Science ®Google Scholar
• Campioni, D., A. Corallini, G. Zauli, L. Possati, G. Altavilla, and J. Barbanti-Brodano 1995. HIV type 1 extracellular Tat protein stimulates growth and protects cells of BK virus/tat transgenic mice from apoptosis. AIDS Res. Hum. Retroviruses 11:1039–1048.
   PubMedGoogle Scholar
• Casolaro, V., S. N. Georas, Z. Song, I. D. Zubkoff, S. A. Abdulkadir, D. Thanos, and J. Ono 1995. Inhibition of NF-AT-dependent transcription by NF-κB: implications for differential gene expression in T helper cell subsets. Proc. Natl. Acad. Sci. USA 92:11623–11627.
   PubMedGoogle Scholar
• Chakravarti, D., V. J. LaMorte, M. C. Nelson, T. Nakajima, I. G. Shulman, H. Juguilon, M. Montminy, and J. Evans 1996. Role of CBP/p300 in nuclear receptor signalling. Nature 383:99–102.
   PubMed Web of Science ®Google Scholar
• Chen, L., J. N. M. Glover, P. G. Hogan, A. Rao, and J. Harrison 1998. Structure of the DNA binding domains from NFAT, Fos and Jun bound to DNA. Nature 392:42–48.
   PubMedGoogle Scholar
• Chiang, C.-M., and J. Roeder 1995. Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science 267:531–536.
   PubMed Web of Science ®Google Scholar
• Cujec, T. P., H. Cho, E. Maldonado, J. Meyer, D. Reinberg, and J. Peterlin 1997. The human immunodeficiency virus transactivator Tat interacts with the RNA polymerase II holoenzyme. Mol. Cell. Biol. 17:1817–1823.
   PubMed Web of Science ®Google Scholar
• Cujec, T. P., H. Okamoto, K. Fujinaga, J. Meyer, H. Chamberlin, D. O. Morgan, and J. Peterlin 1997. The HIV transactivator Tat binds to the CDK-activating kinase and activates the phosphorylation of the carboxy-terminal domain of RNA polymerase II. Genes Dev. 11:2645–2657.
   PubMed Web of Science ®Google Scholar
• DuBridge, R. B., P. Tang, H. C. Hsia, P.-M. Leong, J. H. Miller, and J. Calos 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379–387.
   PubMed Web of Science ®Google Scholar
• Feinberg, M. B., D. Baltimore, and J. Frankel 1991. The role of Tat in the human immunodeficiency virus life cycle indicates a primary effect on transcriptional elongation. Proc. Natl. Acad. Sci. USA 88:4045–4049.
   PubMed Web of Science ®Google Scholar
• Garcia-Rodriguez, C., and J. Rao 1998. Nuclear factor of activated T cells (NFAT)-dependent transactivation regulated by the coactivators P300/CREB binding protein (CBP). J. Exp. Med. 187:2031–2036.
   PubMedGoogle Scholar
• Gaynor, R. B. 1995. Regulation of HIV-1 gene expression by the transactivator protein Tat. Curr. Top. Microbiol. Immunol. 193:51–77.
   PubMedGoogle Scholar
• Hauber, J., A. Perkins, E. P. Heimer, and J. Cullen 1987. Trans-activation of human immunodeficiency virus gene expression is mediated by nuclear events. Proc. Natl. Acad. Sci. USA 84:6364–6368.
   PubMedGoogle Scholar
• Hedin, K. E., M. P. Bell, K. R. Kalli, C. J. Huntoon, B. M. Sharp, and J. Mckean 1997. Delta-opioid receptors expressed by Jurkat T cells enhance IL-2 secretion by increasing AP-1 complexes and activity of the NF-AT/AP-1-binding promoter element. J. Immunol. 159:5431–5440.
   PubMedGoogle Scholar
• Herrmann, C. H., and J. Rice 1995. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxy-terminal domain of the large subunit of RNA-polymerase II: candidate for a Tat cofactor. J. Virol. 69:1612–1620.
   PubMed Web of Science ®Google Scholar
• Ho, A. M., J. Jain, A. Rao, and J. Hogan 1994. Expression of the transcription factor NFATp in a neuronal cell line and in the murine nervous system. J. Biol. Chem. 269:28181–28186.
   PubMedGoogle Scholar
• Hoey, T., Y. L. Sun, K. Williamson, and J. Xu 1995. Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2:461–472.
   PubMed Web of Science ®Google Scholar
• Hottiger, M. O., L. K. Felzien, and J. Nabel 1998. Modulation of cytokine-induced HIV gene expression by competitive binding of transcription factors to the coactivator p300. EMBO J. 17:3124–3134.
   PubMedGoogle Scholar
• Howcroft, T. K., L. A. Palmer, J. Brown, B. Rellahan, F. Kashanchi, J. N. Brady, and J. Singer 1995. HIV Tat represses transcription through Sp1-like elements in the basal promoter. Immunity 3:127–138.
   PubMedGoogle Scholar
• Jacque, J.-M., B. Fernandez, F. Arenzana-Seisdedos, D. Thomas, F. Baleux, J.-L. Virelizier, and J. Bachelerie 1996. Permanent occupancy of the human immunodeficiency virus type 1 enhancer by NF-κB is needed for persistent viral replication in monocytes. J. Virol. 70:2930–2938.
   PubMed Web of Science ®Google Scholar
• Jain, J., E. Burgeon, T. M. Badalian, P. G. Hogan, and J. Rao 1995. A similar DNA-binding motif in NFAT family proteins and the Rel homology region. J. Biol. Chem. 270:4138–4145.
   PubMedGoogle Scholar
• Jain, J., P. G. McCaffrey, Z. Miner, T. K. Kerppola, J. N. Lambert, G. L. Verdine, T. Curran, and J. Rao 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352–355.
   PubMed Web of Science ®Google Scholar
• Jeang, K. T., R. Chun, N. H. Lin, A. Gatignol, C. G. Glabe, and J. Fan 1993. In vitro and in vivo binding of human immunodeficiency virus type 1 Tat protein and Sp1 transcription factor. J. Virol. 67:6224–6233.
   PubMed Web of Science ®Google Scholar
• Jones, K. A., and J. Peterlin 1994. Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem. 63:717–743.
   PubMed Web of Science ®Google Scholar
• Kiani, A., J. P. B. Viola, A. H. Lichtman, and J. Rao 1997. Down-regulation of IL-4 gene transcription and control of Th2 cell differentiation by a mechanism involving NFAT1. Immunity 7:849–860.
   PubMed Web of Science ®Google Scholar
• Kinoshita, S., B. K. Chen, H. Kaneshima, and J. Nolan 1998. Host control of HIV-1 parasitism in T cells by the nuclear factor of activated T cells. Cell 95:595–604.
   PubMedGoogle Scholar
• Kinoshita, S., L. Su, M. Amano, L. A. Timmerman, H. Kaneshima, and J. Nolan 1997. The T cell activation factor NF-ATc positively regulates HIV-1 replication and gene expression in T cells. Immunity 6:235–244.
   PubMed Web of Science ®Google Scholar
• Klein-Hessling, S., G. Schneider, A. Heinfling, S. Chuvpilo, and J. Serfling 1996. HMG I(Y) interferes with the DNA binding of NF-AT factors and the induction of the interleukin 4 promoter in T cells. Proc. Natl. Acad. Sci. USA 93:15311–15316.
   PubMedGoogle Scholar
• Laspia, M. F., A. P. Rice, and J. Mathews 1989. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59:283–292.
   PubMed Web of Science ®Google Scholar
• Li, C. J., C. Wang, D. J. Friedman, and J. Pardee 1995. Reciprocal modulations between p53 and Tat of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 92:5461–5464.
   PubMed Web of Science ®Google Scholar
• Liu, Y.-Z., and J. Latchman 1997. The octamer-binding proteins Oct-1 and Oct-2 repress the HIV long terminal repeat promoter and its transactivation by Tat. Biochem. J. 322:155–158.
   PubMedGoogle Scholar
• Loh, C., K. T. Shaw, J. Carew, J. P. Viola, C. Luo, B. A. Perrino, and J. Rao 1996. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271:10884–10891.
   PubMedGoogle Scholar
• Luo, C., E. Burgeon, J. A. Carew, P. G. McCaffrey, T. M. Badalian, W. Lane, P. G. Hogan, and J. Rao 1996. Recombinant NFAT1 (NFATp) is regulated by calcineurin in T cells and mediates transcription of several cytokine genes. Mol. Cell. Biol. 16:3955–3966.
   PubMed Web of Science ®Google Scholar
• Luo, C., E. Burgeon, and J. Rao 1996. Mechanisms of transactivation by nuclear factor of activated T cells. J. Exp. Med. 184:141–147.
   PubMed Web of Science ®Google Scholar
• Maggirwar, S. B., E. W. Harhaj, and J. Sun 1997. Regulation of the interleukin-2 CD28-responsive element by NF-ATp and various NF-κB/Rel transcription factors. Mol. Cell. Biol. 17:2605–2614.
   PubMed Web of Science ®Google Scholar
• Marciniak, R. A., and J. Sharp 1991. HIV-1 Tat protein promotes formation of more-processive elongation complexes. EMBO J. 10:4189–4196.
   PubMed Web of Science ®Google Scholar
• Masuda, E. S., Y. Naito, H. Tokumitsu, D. Campbell, F. Saito, C. Hannum, K. Arai, and J. Arai 1995. NFATx, a novel member of the NFAT family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15:2697–2706.
   PubMed Web of Science ®Google Scholar
• Mavankal, G., S. H. Ignatius Ou, H. Oliver, D. Sigman, and J. Gaynor 1996. Human immunodeficiency virus type 1 and 2 proteins specifically interact with RNA polymerase II. Proc. Natl. Acad. Sci. USA 93:2089–2094.
   PubMed Web of Science ®Google Scholar
• McCaffrey, P. G., J. Jain, C. Jamieson, R. Sen, and J. Rao 1992. A T cell nuclear factor resembling NF-AT binds to an NF-κB site and to the conserved lymphokine promoter sequence “Cytokine-1.” J. Biol. Chem. 267:1864–1871.
   PubMedGoogle Scholar
• McCaffrey, P. G., C. Luo, T. K. Kerppola, J. Jain, T. M. Badalian, A. M. Ho, E. Burgeon, W. S. Lane, J. N. Lambert, T. Curran, G. L. Verdine, A. Rao, and J. Hogan 1993. Isolation of the cyclosporine-sensitive T cell transcription factor NFATp. Science 262:750–754.
   PubMed Web of Science ®Google Scholar
• Meyaard, L., S. A. Otto, I. P. Keet, R. A. van Lier, and J. Miedema 1994. Changes in cytokine secretion patterns of CD4+ T-cell clones in human immunodeficiency virus infection. Blood 84:4262–4268.
   PubMed Web of Science ®Google Scholar
• Nabel, G., and J. Baltimore 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326:711–713.
   PubMed Web of Science ®Google Scholar
• Northrop, J. P., S. N. Ho, L. Chen, D. J. Thomas, L. A. Timmerman, G. P. Nolan, A. Admon, and J. Crabtree 1994. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369:497–502.
   PubMed Web of Science ®Google Scholar
• Okamoto, H., C. T. Sheline, J. Corden, K. A. Jones, and J. Peterlin 1996. Trans-activation by human immunodeficiency virus Tat protein requires the C-terminal domain of RNA polymerase II. Proc. Natl. Acad. Sci. USA 93:11575–11579.
   PubMedGoogle Scholar
• Ott, M., S. Emiliani, C. Van Lint, G. Herbein, J. Lovett, N. Chirmule, T. McCloskey, S. Pahwa, and J. Verdin 1997. Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 275:1481–1485.
   PubMed Web of Science ®Google Scholar
• Pantaleo, G., and J. Fauci 1995. New concepts in the immunopathogenesis of HIV infection. Annu. Rev. Immunol. 13:487–512.
   PubMed Web of Science ®Google Scholar
• Perkins, N. D., A. B. Agranoff, E. Pascal, and J. Nabel 1994. An interaction between the DNA-binding domain of RelA (p65) and Sp1 mediates human immunodeficiency virus gene activation. Mol. Cell. Biol. 14:6570–6583.
   PubMed Web of Science ®Google Scholar
• Perkins, N. D., N. L. Edwards, C. S. Duckett, A. B. Agranoff, R. M. Schmid, and J. Nabel 1993. A cooperative interaction between NF-κB and Sp1 is required for HIV-1 enhancer activation. EMBO J. 12:3551–3558.
   PubMed Web of Science ®Google Scholar
• Ranger, A. M., M. R. Hodge, E. M. Gravallese, M. Oukka, L. Davidson, F. W. Alt, F. C. Delabrousse, T. Hoey, M. Grusby, and J. Glimcher 1998. Delayed lymphoid repopulation with defects in IL-4-driven responses produced by inactivation of NF-ATC. Immunity 8:125–134.
   PubMed Web of Science ®Google Scholar
• Rao, A. 1994. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today 15:274–281.
   PubMedGoogle Scholar
• Rao, A., C. Luo, and J. Hogan 1997. Transcription factors of the NFAT family—regulation and function. Annu. Rev. Immunol. 15:707–747.
   PubMed Web of Science ®Google Scholar
• Rhim, H., C. O. Echetebu, C. H. Herrmann, and J. Rice 1994. Wild type and mutant HIV-1 and HIV-2 Tat proteins expressed in Escherichia coli as fusions proteins with glutathione S-transferase. J. Acquired Immune Defic. Syndr. 7:1116–1121.
   PubMedGoogle Scholar
• Rooney, J. W., Y. L. Sun, L. H. Glimcher, and J. Hoey 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.
   PubMed Web of Science ®Google Scholar
• Shapiro, V. S., K. E. Truitt, J. B. Imboden, and J. Weiss 1997. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF–IL-2B AP-1 sites. Mol. Cell. Biol. 17:4051–4058.
   PubMed Web of Science ®Google Scholar
• Shaw, K. T.-Y., A. M. Ho, A. Raghavan, J. Kim, J. Jain, J. Park, S. Sharma, A. Rao, and J. Hogan 1995. Immunosuppressive drugs prevent a rapid dephosphorylation of the transcription factor NFAT1 in stimulated immune cells. Proc. Natl. Acad. Sci. USA 92:11205–11209.
   PubMed Web of Science ®Google Scholar
• Sune, C., and J. Garcia-Blanco 1995. Sp1 transcription factor is required for in vitro basal and Tat-activated transcription from the human immunodeficiency virus type 1 long terminal repeat. J. Virol. 69:6572–6576.
   PubMedGoogle Scholar
• Vacca, A., M. Farina, M. Maroder, E. Alesse, I. Screpanti, L. Frati, and J. Gulino 1994. Human immunodeficiency virus type 1 Tat enhances interleukin-2 promoter activity through synergism with phorbol ester and calcium-mediated activation of the NF-AT cis-regulatory motif. Biochem. Biophys. Res. Commun. 205:467–474.
   PubMedGoogle Scholar
• Valgue-Archer, V. E., J. De Villiers, A. J. Sinskey, and J. Rao 1990. Transformation of T lymphocytes by the v-fos oncogene. J. Immunol. 145:4355–4364.
   PubMedGoogle Scholar
• Verhoef, K., M. Koper, and J. Berkhout 1997. Determination of the minimal amount of Tat activity required for human immunodeficiency virus type 1 replication. Virology 237:228–236.
   PubMed Web of Science ®Google Scholar
• Wei, P., M. E. Garber, S. M. Fang, W. H. Fisher, and J. Jones 1998. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high affinity, loop-specific binding to TAR RNA. Cell 92:451–462.
   PubMed Web of Science ®Google Scholar
• Yoo, J., H. Chen, T. Kraus, D. Hirsch, S. Polyak, I. George, and J. Sperber 1996. Altered cytokine production and accessory cell function after HIV-1 infection. J. Immunol. 157:1313–1320.
   PubMed Web of Science ®Google Scholar
• Zhu, Y., T. Pe’ery, J. Peng, Y. Ramanathan, N. Marshall, T. Marshall, B. Amendt, M. B. Mathews, and J. Price 1997. Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 11:2622–2632.
   PubMed Web of Science ®Google Scholar