Reciprocal modulatory interaction between human immunodeficiency virus type 1 tat and transcription factor NFAT1

Molecular and Cellular Biology

Volumn 19, Issue 5, 1999, Pages 3645-3653

  Macián, Fernando ^a   Rao, Anjana ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CENTER FOR BLOOD RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFAT1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LONG TERMINAL REPEAT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS TRANSCRIPTION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 0032908409     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.5.3645     Document Type: Article

References (68)

1. 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 F. Arenzana-Seisdedos. 1995. Absolute dependence on KB responsive elements for initiation and Tat-mediated amplification of HIV transcription in blood CD4+ T lymphocytes. EMBO J. 14:1552-1560.
2. Ambrosino, C., M. R. Ruocco, X. Chen, M. Mallardo, F. Baudi, S. Trematerra, I. Quinto, S. Venuta, and G. 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.
3. Aramburu, J., L. Azzoni, A. Rao, and B. 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.
4. Berkhout, B., and K. T. 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.
5. Blau, J., H. Xiao, S. McCracken, P. O'Hare, J. Greenblatt, and D. Bentley. 1996. Three functional classes of transcriptional activation domains. Mol. Cell. Biol. 16:2044-2055.
6. 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.
7. Buonaguro, L., G. Barillari, H. K. Chang, C. A. Bohan, V. Kao, R. Morgan, R. C. Gallo, and B. Ensoli. 1992. Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines. J. Virol. 66:7159-7167.
8. Campioni, D., A. Corallini, G. Zauli, L. Possati, G. Altavilla, and G. 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.
9. Casolaro, V., S. N. Georas, Z. Song, I. D. Zubkoff, S. A. Abdulkadir, D. Thanos, and S. 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.
10. Chakravarti, D., V. J. LaMorte, M. C. Nelson, T. Nakajima, I. G. Shulman, H. Juguilon, M. Montminy, and R. M. Evans. 1996. Role of CBP/p300 in nuclear receptor signalling. Nature 383:99-102.
11. Chen, L., J. N. M. Glover, P. G. Hogan, A. Rao, and S. C. Harrison. 1998. Structure of the DNA binding domains from NFAT, Fos and Jun bound to DNA. Nature 392:42-48.
12. Chiang, C.-M., and R. G. Roeder. 1995. Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science 267: 531-536.
13. Cujec, T. P., H. Cho, E. Maldonado, J. Meyer, D. Reinberg, and B. M. Peterlin. 1997. The human immunodeficiency virus transactivator Tat interacts with the RNA polymerase II holoenzyme. Mol. Cell. Biol. 17:1817-1823.
14. Cujec, T. P., H. Okamoto, K. Fujinaga, J. Meyer, H. Chamberlin, D. O. Morgan, and B. M. 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.
15. DuBridge, R. B., P. Tang, H. C. Hsia, P.-M. Leong, J. H. Miller, and M. P. Calos. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
16. Feinberg, M. B., D. Baltimore, and A. D. 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.
17. Garcia-Rodriguez, C., and A. 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.
18. Gaynor, R. B. 1995. Regulation of HIV-1 gene expression by the transactivator protein Tat. Curr. Top. Microbiol. Immunol. 193:51-77.
19. Hauber, J., A. Perkins, E. P. Heimer, and B. R. Cullen. 1987. Trans-activation of human immunodeficiency virus gene expression is mediated by nuclear events. Proc. Natl. Acad. Sci. USA 84:6364-6368.
20. Hedin, K. E., M. P. Bell, K. R. Kalli, C. J. Huntoon, B. M. Sharp, and D. 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.
21. Herrmann, C. H., and A. P. 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.
22. Ho, A. M., J. Jain, A. Rao, and P. G. 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.
23. Hoey, T., Y. L. Sun, K. Williamson, and X. 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.
24. Hottiger, M. O., L. K. Felzien, and J. N. Nabel. 1998. Modulation of cytokine-induced HIV gene expression by competitive binding of transcription factors to the coactivator p300. EMBO J. 17:3124-3134.
25. Howcroft, T. K., L. A. Palmer, J. Brown, B. Rellahan, F. Kashanchi, J. N. Brady, and D. S. Singer. 1995. HIV Tat represses transcription through Sp1-like elements in the basal promoter. Immunity 3:127-138.
26. Jacque, J.-M., B. Fernandez, F. Arenzana-Selsdedos, D. Thomas, F. Baleux, J.-L. Virelizier, and F. 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.
27. Jain, J., E. Burgeon, T. M. Badalian, P. G. Hogan, and A. Rao. 1995. A similar DNA-binding motif in NFAT family proteins and the Rel homology region. J. Biol. Chem. 270:4138-4145.
28. Jain, J., P. G. McCaffrey, Z. Miner, T. K. Kerppola, J. N. Lambert, G. L. Verdine, T. Curran, and A. Rao. 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352-355.
29. Jeang, K. T., R. Chun, N. H. Lin, A. Gatignol, C. G. Glabe, and H. 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.
30. Jones, K. A., and B. M. Peterlin. 1994. Control of RNA initiation and elongation at the HIV-1 promoter. Annu. Rev. Biochem. 63:717-743.
31. Kiani, A., J. P. B. Viola, A. H. Lichtman, and A. Rao. 1997. Down-regulation of IL-4 gene transcription and control of Th2 cell differentiation by a mechanism involving NFAT1. Immunity 7:849-860.
32. Kinoshita, S., B. K. Chen, H. Kaneshima, and G. P. Nolan. 1998. Host control of HIV-1 parasitism in T cells by the nuclear factor of activated T cells. Cell 95:595-604.
33. Kinoshila, S., L. Su, M. Amano, L. A. Timmerman, H. Kaneshima, and G. P. Nolan. 1997. The T cell activation factor NF-ATc positively regulates HIV-1 replication and gene expression in T cells. Immunity 6:235-244.
34. Klein-Hessling, S., G. Schneider, A. Heinfling, S. Chuvpilo, and E. 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.
35. Laspia, M. F., A. P. Rice, and M. B. Mathews. 1989. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59:283-292.
36. Li, C. J., C. Wang, D. J. Friedman, and A. B. Pardee. 1995. Reciprocal modulations between p53 and Tat of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 92:5461-5464.
37. Liu, Y.-Z., and D. S. 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.
38. Loh, C., K. T. Shaw, J. Carew, J. P. Viola, C. Luo, B. A. Perrino, and A. Rao. 1996. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271:10884-10891.
39. Luo, C., E. Burgeon, J. A. Carew, P. G. McCaffrey, T. M. Badalian, W. Lane, P. G. Hogan, and A. 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.
40. Luo, C., E. Burgeon, and A. Rao. 1996. Mechanisms of transactivation by nuclear factor of activated T cells. J. Exp. Med. 184:141-147.
41. Maggirwar, S. B., E. W. Harhaj, and S.-C. 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.
42. Marciniak, R. A., and P. A. Sharp. 1991. HIV-1 Tat protein promotes formation of more-processive elongation complexes. EMBO J. 10:4189-4196.
43. Masuda, E. S., Y. Naito, H. Tokumitsu, D. Campbell, F. Saito, C. Hannum, K. Aral, and N. Aral. 1995. NFATx, a novel member of the NFAT family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15:2697-2706.
44. Mavankal, G., S. H. Ignatius Ou, H. Oliver, D. Sigman, and R. B. Gaynor. 1996. Human immunodeficiency virus type 1 and 2 proteins specifically interact with RNA polymerase II. Proc. Natl. Acad. Sci. USA 93:2089-2094.
45. McCaffrey, P. G., J. Jain, C. Jamieson, R. Sen, and A. 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.
46. 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 P. G. Hogan. 1993. Isolation of the cyclosporine-sensitive T cell transcription factor NFATp. Science 262:750-754.
47. Meyaard, L., S. A. Otto, I. P. Keet, R. A. van Lier, and F. Miedema. 1994. Changes in cytokine secretion patterns of CD4+ T-cell clones in human immunodeficiency virus infection. Blood 84:4262-4268.
48. Nabel, G., and D. Baltimore. 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326: 711-713.
49. Northrop, J. P., S. N. Ho, L. Chen, D. J. Thomas, L. A. Timmerman, G. P. Nolan, A. Admon, and G. R. Crabtree. 1994. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369:497-502.
50. Okamoto, H., C. T. Sheline, J. Corden, K. A. Jones, and B. M. 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.
51. Ott, M., S. Emiliani, C. Van Lint, G. Herbein, J. Lovett, N. Chirmule, T. McCloskey, S. Pahwa, and E. Verdin. 1997. Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 275:1481-1485.
52. Pantaleo, G., and A. S. Fauci. 1995. New concepts in the immunopathogenesis of HIV infection. Annu. Rev. Immunol. 13:487-512.
53. Perkins, N. D., A. B. Agranoff, E. Pascal, and G. 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.
54. Perkins, N. D., N. L. Edwards, C. S. Duckett, A. B. Agranoff, R. M. Schmid, and G. J. Nabel. 1993. A cooperative interaction between NF-κB and Sp1 is required for HIV-1 enhancer activation. EMBO J. 12:3551-3558.
55. Ranger, A. M. M. R. Hodge, E. M. Gravallese, M. Oukka, L. Davidson, F. W. Alt, F. C. Delabrousse, T. Hoey, M. Grusby, and L. H. Glimcher. 1998. Delayed lymphoid repopulation with defects in IL-4-driven responses produced by inactivation of NF-ATC. Immunity 8:125-134.
56. Ran, A. 1994. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today 15:274-281.
57. Rao, A., C. Luo, and P. G. Hogan. 1997. Transcription factors of the NFAT family - regulation and function. Annu. Rev. Immunol. 15:707-747.
58. Rhim, H., C. O. Echetebu, C. H. Herrmann, and A. P. 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.
59. Rooney, J. W., Y. L. Sun, L. H. Glimcher, and T. 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.
60. Shapiro, V. S., K. E. Truitt, J. B. Imboden, and A. 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.
61. Shaw, K. T.-Y., A. M. Ho, A. Raghavan, J. Kim, J. Jain, J. Park, S. Sharma, A. Rao, and P. G. 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.
62. Sune, C., and M. A. 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.
63. Vacca, A., M. Farina, M. Maroder, E. Alesse, I. Screpanti, L. Frati, and A. 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.
64. Valgue-Archer, V. E., J. De Villiers, A. J. Sinskey, and A. Rao. 1990. Transformation of T lymphocytes by the v-fos oncogene. J. Immunol. 145:4355-4364.
65. Verhoef, K., M. Koper, and B. Berkhout. 1997. Determination of the minimal amount of Tat activity required for human immunodeficiency virus type 1 replication. Virology 237:228-236.
66. Wel, P., M. E. Garber, S. M. Fang, W. H. Fisher, and K. A. 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.
67. Yoo, J., H. Chen, T. Kraus, D. Hirsch, S. Polyak, I. George, and K. Sperber. 1996. Altered cytokine production and accessory cell function after HIV-1 infection. J. Immunol. 157:1313-1320.
68. Zhu, Y., T. Pe'ery, J. Peng, Y. Ramanathan, N. Marshall, T. Marshall, B. Amendt, M. B. Mathews, and D. H. Price. 1997. Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 11:2622-2632.