1887

Abstract

Human immunodeficiency virus type 1 (HIV-1) Tat affects cellular gene expression through modulation of the activity of different transcription factors. Here, the role of Tat in the cooperation between nuclear factor of activated T cells (NFAT) and activator protein 1 (AP-1) transcription factors was investigated. Constitutive or transient Tat expression in Jurkat T cells enhanced cooperative NFAT/AP-1- but not AP-1-dependent transcription independent of its ability to transactivate the HIV-1 LTR. The enhancing effect of Tat took place after nuclear translocation of NFAT. Furthermore, transactivation of an NFAT/AP-1 reporter by transfection of NFAT and c-Jun was strongly enhanced by simultaneous Tat transfection. Moreover, intracellular Tat expression increased the binding of NFAT/AP-1 complexes to the interleukin 2 promoter without significantly altering NFAT- and AP-1-independent binding. HIV-1 Tat interacted with NFAT but not c-Jun. These results indicate that Tat interacts with NFAT, affecting its cooperation with AP-1, without altering independent binding of these transcription factors to DNA.

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2006-06-01
2019-10-23
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References

  1. Abraham, S., Sweet, T., Sawaya, B. E., Rappaport, J., Khalili, K. & Amini, S. ( 2005; ). Cooperative interaction of C/EBPβ and Tat modulates MCP-1 gene transcription in astrocytes. J Neuroimmunol 160, 219–227.[CrossRef]
    [Google Scholar]
  2. Ambrosino, C., Ruocco, M. R., Chen, X., Mallardo, M., Baudi, F., Trematerra, S., Quinto, I., Venuta, S. & Scala, G. ( 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 β (NF-IL6) transcription factors. J Biol Chem 272, 14883–14892.[CrossRef]
    [Google Scholar]
  3. Ambrosino, C., Palmieri, C., Puca, A. & 9 other authors ( 2002; ). Physical and functional interaction of HIV-1 Tat with E2F-4, a transcriptional regulator of mammalian cell cycle. J Biol Chem 277, 31448–31458.[CrossRef]
    [Google Scholar]
  4. Arenzana-Seisdedos, F., Fernandez, B., Dominguez, I., Jacque, J. M., Thomas, D., Diaz-Meco, M. T., Moscat, J. & Virelizier, J. L. ( 1993; ). Phosphatidylcholine hydrolysis activates NF-κB and increases human immunodeficiency virus replication in human monocytes and T lymphocytes. J Virol 67, 6596–6604.
    [Google Scholar]
  5. Aune, T. M. & Flavell, R. A. ( 1997; ). Differential expression of transcription directed by a discrete NF-AT binding element from the IL-4 promoter in naive and effector CD4 T cells. J Immunol 159, 36–43.
    [Google Scholar]
  6. Biswas, D. K., Salas, T. R., Wang, F., Ahlers, C. M., Dezube, B. J. & Pardee, A. B. ( 1995; ). A Tat-induced auto-up-regulatory loop for superactivation of the human immunodeficiency virus type 1 promoter. J Virol 69, 7437–7444.
    [Google Scholar]
  7. Blazquez, M. V., Macho, A., Ortiz, C., Lucena, C., Lopez-Cabrera, M., Sanchez-Madrid, F. & Munoz, E. ( 1999; ). Extracellular HIV type 1 Tat protein induces CD69 expression through NF-kappaB activation: possible correlation with cell surface Tat-binding proteins. AIDS Res Hum Retroviruses 15, 1209–1218.[CrossRef]
    [Google Scholar]
  8. Buonaguro, L., Barillari, G., Chang, H. K., Bohan, C. A., Kao, V., Morgan, R., Gallo, R. C. & Ensoli, B. ( 1992; ). Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines. J Virol 66, 7159–7167.
    [Google Scholar]
  9. Centlivre, M., Sommer, P., Michel, M. & 8 other authors ( 2005; ). HIV-1 clade promoters strongly influence spatial and temporal dynamics of viral replication in vivo. J Clin Invest 115, 348–358.[CrossRef]
    [Google Scholar]
  10. Cullen, B. R. ( 1998; ). HIV-1 auxiliary proteins: making connections in a dying cell. Cell 93, 685–692.[CrossRef]
    [Google Scholar]
  11. Demarchi, F., Gutierrez, M. I. & Giacca, M. ( 1999; ). Human immunodeficiency virus type 1 Tat protein activates transcription factor NF-κB through the cellular interferon-inducible, double-stranded RNA-dependent protein kinase, PKR. J Virol 73, 7080–7086.
    [Google Scholar]
  12. Deng, T. & Karin, M. ( 1993; ). JunB differs from c-Jun in its DNA-binding and dimerization domains and represses c-Jun by formation of inactive heterodimers. Genes Dev 7, 479–490.[CrossRef]
    [Google Scholar]
  13. Durand, D. B., Shaw, J. P., Bush, M. R., Replogle, R. E., Belagaje, R. & Crabtree, G. R. ( 1988; ). Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol Cell Biol 8, 1715–1724.
    [Google Scholar]
  14. Frankel, A. D. & Pabo, C. O. ( 1988; ). Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55, 1189–1193.[CrossRef]
    [Google Scholar]
  15. Ghosh, S., May, M. J. & Kopp, E. B. ( 1998; ). NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16, 225–260.[CrossRef]
    [Google Scholar]
  16. González, E., Punzón, C., González, M. & Fresno, M. ( 2001; ). HIV-1 Tat inhibits IL-2 gene transcription through qualitative and quantitative alterations of the cooperative Rel/AP1 complex bound to the CD28RE/AP1 composite element of the IL-2 promoter. J Immunol 166, 4560–4569.[CrossRef]
    [Google Scholar]
  17. Hauber, J., Perkins, A., Heimer, E. P. & Cullen, B. R. ( 1987; ). Trans-activation of human immunodeficiency virus gene expression is mediated by nuclear events. Proc Natl Acad Sci U S A 84, 6364–6368.[CrossRef]
    [Google Scholar]
  18. Hogan, P. G., Chen, L., Nardone, J. & Rao, A. ( 2003; ). Transcriptional regulation by calcium, calcineurin and NFAT. Genes Dev 17, 2205–2232.[CrossRef]
    [Google Scholar]
  19. Im, S.-H. & Rao, A. ( 2004; ). Activation and deactivation of gene expression by Ca2+/calcineurin-NFAT-mediated signaling. Mol Cells 18, 1–9.
    [Google Scholar]
  20. Íñiguez, M. A., Martinez-Martínez, S., Punzón, C., Redondo, J. M. & Fresno, M. ( 2000; ). An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J Biol Chem 275, 23627–23635.[CrossRef]
    [Google Scholar]
  21. Izmailova, E., Bertley, F. M. N., Huang, Q., Makori, N., Miller, C. J., Young, R. A. & Aldovini, A. ( 2003; ). HIV-1 Tat reprograms immature dendritic cells to express chemoattractants for activated T cells and macrophages. Nat Med 9, 191–197.[CrossRef]
    [Google Scholar]
  22. Jain, J., Miner, Z. & Rao, A. ( 1993; ). Analysis of the preexisting and nuclear forms of nuclear factor of activated T cells. J Immunol 151, 837–848.
    [Google Scholar]
  23. Jeang, K.-T., Chun, R., Lin, N. H., Gatignol, A., Glabe, C. G. & Fan, H. ( 1993; ). In vitro and in vivo binding of human immunodeficiency virus type 1 Tat protein and Sp1 transcription factor. J Virol 67, 6224–6233.
    [Google Scholar]
  24. Jeang, K.-T., Xiao, H. & Rich, E. A. ( 1999; ). Multifaceted activities of the HIV-1 transactivator of transcription, Tat. J Biol Chem 274, 28837–28840.[CrossRef]
    [Google Scholar]
  25. Jeeninga, R. E., Hoogenkamp, M., Armand-Ugon, M., de Baar, M., Verhoef, K. & Berkhout, B. ( 2000; ). Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. J Virol 74, 3740–3751.[CrossRef]
    [Google Scholar]
  26. Johnson, B. V., Bert, A. G., Ryan, G. R., Condina, A. & Cockerill, P. N. ( 2004; ). Granulocyte-macrophage colony-stimulating factor enhancer activation requires cooperation between NFAT and AP-1 elements and is associated with extensive nucleosome reorganization. Mol Cell Biol 24, 7914–7930.[CrossRef]
    [Google Scholar]
  27. Karin, M., Liu, Z. & Zandi, E. ( 1997; ). AP-1 function and regulation. Curr Opin Cell Biol 9, 240–246.[CrossRef]
    [Google Scholar]
  28. Kel, A., Kel-Margoulis, O., Babenko, V. & Wingender, E. ( 1999; ). Recognition of NFATp/AP-1 composite elements within genes induced upon the activation of immune cells. J Mol Biol 288, 353–376.[CrossRef]
    [Google Scholar]
  29. Kumar, A., Manna, S. K., Dhawan, S. & Aggarwal, B. B. ( 1998; ). HIV-Tat protein activates c-Jun N-terminal kinase and activator protein-1. J Immunol 161, 776–781.
    [Google Scholar]
  30. Li, C. J., Ueda, Y., Shi, B., Borodyansky, L., Huang, L., Li, Y.-Z. & Pardee, A. B. ( 1997; ). Tat protein induces self-perpetuating permissivity for productive HIV-1 infection. Proc Natl Acad Sci U S A 94, 8116–8120.[CrossRef]
    [Google Scholar]
  31. Lim, S. P. & Garzino-Demo, A. ( 2000; ). The human immunodeficiency virus type 1 Tat protein up-regulates the promoter activity of the beta-chemokine monocyte chemoattractant protein 1 in the human astrocytoma cell line U-87 MG: role of SP-1, AP1 and NF-κB consensus sites. J Virol 74, 1632–1640.[CrossRef]
    [Google Scholar]
  32. Macián, F. & Rao, A. ( 1999; ). Reciprocal modulatory interaction between human immunodeficiency virus type 1 Tat and transcription factor NFAT1. Mol Cell Biol 19, 3645–3653.
    [Google Scholar]
  33. Macián, F., López-Rodríguez, C. & Rao, A. ( 2001; ). Partners in transcription: NFAT and AP-1. Oncogene 20, 2476–2489.[CrossRef]
    [Google Scholar]
  34. Navarro, J., Punzón, C., Jiménez, J. L., Fernández-Cruz, E., Pizarro, A., Fresno, M. & Muñoz-Fernández, M. A. ( 1998; ). Inhibition of phosphodiesterase type IV suppresses human immunodeficiency virus type 1 replication and cytokine production in primary T cells: involvement of NF-κB and NFAT. J Virol 72, 4712–4720.
    [Google Scholar]
  35. Nolan, G. P. ( 1994; ). NF-AT-AP-1 and Rel-bZIP: hybrid vigor and binding under the influence. Cell 77, 795–798.[CrossRef]
    [Google Scholar]
  36. Ott, M., Lovett, J. L., Mueller, L. & Verdin, E. ( 1998; ). Superinduction of IL-8 in T cells by HIV-1 Tat protein is mediated through NF-κB factors. J Immunol 160, 2872–2880.
    [Google Scholar]
  37. Park, J., Yaseen, N. R., Hogan, P. G., Rao, A. & Sharma, S. ( 1995; ). Phosphorylation of the transcription factor NFATp inhibits its DNA binding activity in cyclosporin A-treated human B and T cells. J Biol Chem 270, 20653–20659.[CrossRef]
    [Google Scholar]
  38. Peterson, B. R., Sun, L. J. & Verdine, G. L. ( 1996; ). A critical arginine residue mediates cooperativity in the contact interface between transcription factors NFAT and AP-1. Proc Natl Acad Sci U S A 93, 13671–13676.[CrossRef]
    [Google Scholar]
  39. Rowland-Jones, S. L. ( 2003; ). Timeline: AIDS pathogenesis: what have two decades of HIV research taught us? Nat Rev Immunol 3, 343–348.[CrossRef]
    [Google Scholar]
  40. Schwartz, O., Virelizier, J.-L., Montagnier, L. & Hazan, U. ( 1990; ). A microtransfection method using the luciferase-encoding reporter gene for the assay of human immunodeficiency virus LTR promoter activity. Gene 88, 197–205.[CrossRef]
    [Google Scholar]
  41. Shaw, J. P., Utz, P. J., Durand, D. B., Toole, J. J., Emmel, E. A. & Crabtree, G. R. ( 1988; ). Identification of a putative regulator of early T cell activation genes. Science 241, 202–205.[CrossRef]
    [Google Scholar]
  42. Stevenson, M. ( 2003; ). HIV-1 pathogenesis. Nat Med 9, 853–860.[CrossRef]
    [Google Scholar]
  43. Sun, L. J., Peterson, B. R. & Verdine, G. L. ( 1997; ). Dual role of the nuclear factor of activated T cells insert region in DNA recognition and cooperative contacts to activator protein 1. Proc Natl Acad Sci U S A 94, 4919–4924.[CrossRef]
    [Google Scholar]
  44. Truant, R. & Cullen, B. R. ( 1999; ). The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin β-dependent nuclear localization signals. Mol Cell Biol 19, 1210–1217.
    [Google Scholar]
  45. Vacca, A., Farina, M., Maroder, M., Alesse, E., Screpanti, I., Frati, L. & Gulino, A. ( 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.[CrossRef]
    [Google Scholar]
  46. van Opijnen, T., Jeeninga, R. E., Boerlijst, M. C., Pollakis, G. P., Zetterberg, V., Salminen, M. & Berkhout, B. ( 2004; ). Human immunodeficiency virus type 1 subtypes have a distinct long terminal repeat that determines the replication rate in a host-cell-specific manner. J Virol 78, 3675–3683.[CrossRef]
    [Google Scholar]
  47. Verhoef, K. & Berkhout, B. ( 1999; ). A second-site mutation that restores replication of a Tat-defective human immunodeficiency virus. J Virol 73, 2781–2789.
    [Google Scholar]
  48. Weiss, C., Schneider, S., Wagner, E. F., Zhang, X., Seto, E. & Bohmann, D. ( 2003; ). JNK phosphorylation relieves HDAC3-dependent suppression of the transcriptional activity of c-Jun. EMBO J 22, 3686–3695.[CrossRef]
    [Google Scholar]
  49. Westendorp, M. O., Li-Weber, M., Frank, R. W. & Krammer, P. H. ( 1994; ). Human immunodeficiency virus type 1 Tat upregulates interleukin-2 secretion in activated T cells. J Virol 68, 4177–4185.
    [Google Scholar]
  50. Yang, T. T. C. & Chow, C.-W. ( 2003; ). Transcription cooperation by NFAT.C/EBP composite enhancer complex. J Biol Chem 278, 15874–15885.[CrossRef]
    [Google Scholar]
  51. Yang, Y., Dong, B., Mittelstadt, P. R., Xiao, H. & Ashwell, J. D. ( 2002; ). HIV Tat binds Egr proteins and enhances Egr-dependent transactivation of the Fas ligand promoter. J Biol Chem 277, 19482–19487.[CrossRef]
    [Google Scholar]
  52. Zagury, D., Lachgar, A., Chams, V. & 10 other authors ( 1998; ). Interferon α and Tat involvement in the immunosuppression of uninfected T cells and C-C chemokine decline in AIDS. Proc Natl Acad Sci U S A 95, 3851–3856.[CrossRef]
    [Google Scholar]
  53. Zauli, G., Davis, B. R., Re, M. C., Visani, G., Furlini, G. & La Place, M. ( 1992; ). tat protein stimulates production of transforming growth factor-β1 by marrow macrophages: a potential mechanism for human immunodeficiency virus-1-induced hematopoietic suppression. Blood 80, 3036–3043.
    [Google Scholar]
  54. Zhu, C., Rao, K., Xiong, H., Gagnidze, K., Li, F., Horvath, C. & Plevy, S. ( 2003; ). Activation of the murine interleukin-12 p40 promoter by functional interactions between NFAT and ICSBP. J Biol Chem 278, 39372–39382.[CrossRef]
    [Google Scholar]
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