The hepatitis B virus X protein activates nuclear factor of activated T cells (NF-AT) by a cyclosporin A-sensitive pathway

EMBO Journal

Volumn 17, Issue 23, 1998, Pages 7066-7077

  Lara Pezzi, Enrique ^a   Armesilla, Angel Luis ^b   Majano, Pedro L ^a   Redondo, Juan Miguel ^b   López Cabrera, Manuel ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CSIC   (Spain)

Author keywords

Cyclosporin A; HBx; Hepatitis B virus; NF AT; Transcription

Indexed keywords

CELL DNA; CYCLOSPORIN A; LUCIFERASE; NUCLEAR FACTOR; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DEPHOSPHORYLATION; DRUG SENSITIVITY; GENE EXPRESSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; T LYMPHOCYTE ACTIVATION; TRANSACTIVATION;

HEPATITIS B VIRUS;

EID: 0032403765     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.23.7066     Document Type: Article

References (68)

1. Andus, T., Bauer, J. and Gerok, W. (1991) Effects of cytokines on the liver. Hepatology, 13, 364-375.
2. Benn, J. and Schneider, R.J. (1994) Hepatitis virus HBx protein activates Ras-GTP complex formation and establishes a Ras, Raf, MAP kinase signalling cascade. Proc. Natl Acad. Sci. USA, 91, 10350-10354.
3. Benn, J., Su, F., Doria, M. and Schneider, R.J. (1996) Hepatitis B virus HBx protein induces transcription factor AP-1 by activation of extracellular signal-regulated and c-jun N-terminal mitogen-activated protein kinases. J. Virol., 70, 4978-4985.
4. Boise, L.H. et al. (1993) The NFAT-1 DNA binding complex in activated T cells contains Fra-1 and JunB. Mol. Cell. Biol., 13, 1911-1919.
5. Cantrell, D. (1996) T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol., 14, 259-274.
6. 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-κB: implications for differential gene expression in T helper cell subsets. Proc. Natl Acad. Sci. USA, 92, 11623-11627.
7. Cheong, J., Yi, M., Lin, Y. and Murakami, S. (1995) Human RPB5, a subunit shared by eukaryotic nuclear RNA polymerases, binds human hepatitis B virus X protein and may play a role in X transactivation. EMBO J., 14, 143-150.
8. Chirillo, P., Falco, M., Puri, P.L., Artini, M., Balsano, C., Levrero, M. and Natoli, G. (1996) Hepatitis B virus pX activates NF-κB dependent transcription through a Raf-independent pathway. J. Virol., 70, 641-646.
9. Chirillo, P., Pagano, S., Natoli, G., Puri, P.L., Burgio, V.L., Balsano, C. and Levrero, M. (1997) The hepatitis B virus pX gene induces p53-mediated programmed cell death. Proc. Natl Acad. Sci. USA, 94, 8162-8167.
10. Chisari, F. and Ferrari, C. (1995) Hepatitis B virus immunopathogenesis. Annu. Rev. Immunol., 13, 29-60.
11. Cockeril, P.N., Bert, A.G., Jenkins, F., Ryan, G.R., Shannon, M.F. and Vadas, M.A. (1995) Human granulocyte-macrophage colony-stimulating factor enhancer function is associated with cooperative interactions between AP-1 and NFATp/c. Mol. Cell. Biol., 15, 2071-2079.
12. Cope, A.P., Liblau, R.S., Yang, X.-D., Congia, M., Laudanna, C., Schreiber, R.D., Probert, L., Kollias, G. and McDevitt, H.O. (1997) Chronic tumor necrosis factor alters T cell responses attenuating T cell receptor signaling. J. Exp. Med., 185, 1573-1584.
13. Crabtree, G.R. and Clipstone, N.A. (1994) Signal transmission between the plasma membrane and the nucleus of T lymphocytes. Annu. Rev. Biochem., 63, 1045-1083.
14. Cross, J., Wen, P. and Rutter, W. (1993) Transactivation by hepatitis B virus X protein is promiscuous and dependent on mitogen-activated cellular serine/threonine kinases. Proc. Natl Acad. Sci. USA, 90, 8078-8082.
15. Doria, M., Klein, N., Lucito, R. and Schneider, R.J. (1995) The hepatitis B virus HBx protein is a dual specificity cytoplasmic activator of Ras and nuclear activator of transcription factors. EMBO J., 14, 4747-4757.
16. Durand, D.B., Shaw, J.-P., Bush, M.R., Replogle, R.E., Belagaje, R. and Crabtree, G.R. (1988) Characterization of antigen receptor response elements within the IL-2 enhancer. Mol. Cell. Biol., 8, 1715-1724.
17. Ferrari, C., Pilli, M., Penna, A., Bertoletti, A., Valli, A., Cavalli, A., Pasetti, G. and Fiaccadori, F. (1992) Autopresentation of hepatitis B virus envelope antigens by T cells. J. Virol., 66, 2536-2540.
18. Franco, A., Paroli, M., Testa, U., Benvenuto, R., Peschle, C., Balsano, F. and Barnaba, V. (1992) Transferrin receptor mediates up-take and presentation of hepatitis B envelope antigens by T cells. J. Exp. Med., 175, 1195-1205.
19. Fukuda, R., Satoh, S., Nguyen, X.T., Uchida, Y., Kohge, N., Akagi, S., Ikeda, S., Watanabe, M. and Fukmoto, S. (1995) Expression rare of cytokine mRNA in the liver of chronic hepatitis C: comparison with chronic hepatitis B. J. Gastroenterol., 30, 41-47.
20. Ganem, D. and Varmus, H.E. (1987) The molecular biology of the hepatitis B virus. Annu. Rev. Biochem., 56, 651-693.
21. Ghosh, P., Sica, A., Cippitelli, M., Subleski, J., Lahesmaa, R., Young, H.A. and Rice, N.R. (1996) Activation of nuclear factor of activated T cells in a cyclosporin A-resistant pathway. J. Biol. Chem., 271, 7700-7704.
22. González-Amaro, R. et al. (1994) Induction of tumor necrosis factor-α production by human hepatocytes in chronic viral hepatitis. J. Exp. Med., 179, 841-848.
23. Good, L., Maggirwar, S.B. and Sun, S.-C. (1996) Activation of the IL-2 gene promoter by HTLV-I Tax involves induction of NF-AT complexes bound to the CD28-responsive element. EMBO J., 15, 3744-3750.
24. Good, L., Maggirwar, S.B., Harhaj, E.W. and Sun, S.-C. (1997) Constitutive dephosphorylation and activation of a member of the nuclear factor of activated T cells, NF-AT1, in Tax-expressing and type I human T-cell leukemia virus-infected human T cells. J. Biol. Chem., 272, 1425-1428.
25. Haviv, I., Vaizel, D. and Shaul, Y. (1995) The X protein of hepatis B virus coactivates potent activation domains. Mol. Cell. Biol., 15, 1079-1085.
26. Haviv, I., Vaizel, D. and Shaul, Y. (1996) pX, the HBV-encoded coactivator, interacts with components of the transcription machinery and stimulates transcription in a TAF-independent manner. EMBO J., 15, 3413-3420.
27. Haviv, I., Shamay, M., Doitsh, G. and Shaul, Y. (1998) Hepatitis B virus pX targets TFIIB in transcription coactivation. Mol. Cell. Biol., 18, 1562-1569.
28. 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 of calcineurin and interacts with Fos and Jun. Nature, 365, 352-355.
29. Jain, J., Loh, C. and Rao, A. (1995) Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol., 7, 333-342.
30. Kekulé, A., Lauer, U., Weiss, L., Luber, B. and Hofsschneider, P. (1993) Hepatitis B virus transactivator HBx uses a tumour promoter signalling pathway. Nature, 361, 742-745.
31. Kieran, M. et al. (1990) The DNA binding subunit of NF-κB is identical to factor κBF1 and homologous to rel oncogene product. Cell, 62, 1007-1018.
32. Kinoshita, S., Su, L., Amano, M., Timmerman, L.A., Kaneshima, H. and Nolan, G.P. (1997) The T cell activation factor NF-ATc positively regulates HIV-1 replication and gene expression in T cells. Immunity, 6, 235-244.
33. Klein, N.P. and Schneider, R.J. (1997) Activation of Src family kinases by hepatitis B virus HBx protein and coupled signaling to Ras. Mol. Cell. Biol., 17, 6427-6436.
34. Koike, K. (1995) Hepatitis B virus HBx gene and hepatocarcinogenesis. Intervirology, 38, 134-142.
35. Lara-Pezzi, E., Majano, P.L., Gómez-Gonzalo, M., García-Monzón, C., Moreno-Otero, R., Levrero, M. and López-Cabrera, M. (1998) The hepatitis B virus X protein up-regulates tumor necrosis factor-α gene expression in hepatocytes. Hepatology, 28, 1013-1021.
36. Lin, Y., Nomura, T., Cheong, J.H., Dorjsuren, D., Iida, K. and Murakami, S. (1997) Hepatitis B virus X protein is a transcriptional modulator that communicates with transcription factor IIB and the RNA polymerase II subunit 5. J. Biol. Chem., 272, 7132-7139.
37. Loh, C., Shaw, K.T.-Y., Carew, J., Viola, J.P.B., Luo, C., Perrino, B.A. and Rao, A. (1996) Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem., 271, 10884-10891.
38. Luo, C., Burgeon, E. and Rao, A. (1996a) Mechanisms of transactivation by nuclear factor of activated T cells 1. J. Exp. Med., 184, 141-147.
39. Luo, C., Shaw, K.T.-Y., Raghavan, A., Aramburu, J., García-Cozar, F., Perrino, B.A., Hogan, P.G. and Rao, A. (1996b) Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc. Natl Acad. Sci. USA, 93, 8907-8912.
40. Lyakh, L., Ghosh, P. and Rice, N.R. (1997) Expression of NFAT-family proteins in normal human T cells. Mol. Cell. Biol., 17, 2475-2484.
41. Maguire, H.F., Hoeffler, J.P. and Siddiqui, A. (1991) HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science, 252, 842-844.
42. Mahé, Y. Mukaida, N., Kuno, K., Akiyama, M., Ikeda, N., Matsushima, K. and Murakami, S. (1991) Hepatitis B virus X protein transactivates human interleukin-8 gene through acting on nuclear factor κB and CCAAT/enhancer-binding protein-like cis-element. J. Biol. Chem., 266, 13759-13763.
43. Martínez-Martínez, S., Arco, P.G.D., Armesilla, A.L., Aramburu, J., Luo, C., Rao, A. and Redondo, J.M. (1997) Blockade of T-cell activation by dithiocarbamates involves novel mechanisms of inhibition of nuclear factor of activated T cells. Mol. Cell. Biol., 17, 6437-6447.
44. Minden, A., Lin, A., Claret, F.-X., Abo, A. and Karin, M. (1995) Selective activation of the JNK signalling cascade and c-jun transcriptional activity by the small GTPases Rac and cdc42Hs. Cell, 81, 1147-1157.
45. Murakami, S., Cheong, J., Ohno, S., Matsushima, K. and Kaneko, S. (1994) Transactivation of human hepatitis B virus X protein, HBx, operates through a mechanism distinct from protein kinase C and okadaic acid activation pathways. Virology, 199, 243-246.
46. Natoli, G., Avantaggiati, M., Chirillo, P., Constanzo, A., Artini, M., Balsano, C. and Levrero, M. (1994a) Induction of the DNA-binding activity of c-Jun/c-Fos heterodimers by the hepatitis B virus transactivator pX. Mol. Cell. Biol., 14, 989-998.
47. Natoli, G., Avantaggiati, M., Chirillo, P., Puri, P., Ianni, A., Balsano, C. and Levrero, M. (1994b) Ras-and Raf-dependent activation of c-jun transcriptional activity by hepatitis B virus transactivator pX. Oncogene, 9, 2836-2843.
48. Northrop, J.P., Ullman, K.S. and Crabtree, G.R. (1993) Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells. J. Biol. Chem., 268, 2917-2923.
49. 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, 369, 497-502.
50. Okamoto, S.-I., Mukaida, N., Yasumoto, K., Rice, N., Ishikawa, Y., Horiguchi, H., Murakami, S. and Matsushima, K. (1994) The interleukin-8 AP-1 and κB-like sites are genetic end targets of FK506-sensitive pathway accompanied by calcium mobilization. J. Biol. Chem., 269, 8582-8589.
51. Qadri, I., Maguire, H. and Siddiqui, A. (1995) Hepatitis B virus transactivator protein X interacts with the TATA-binding protein. Proc. Natl Acad. Sci. USA, 92, 1003-1007.
52. Rao, A. (1994) NFATp: a transcription factor required for the coordinated induction of several cytokine genes. Immunol. Today, 15, 274-281.
53. Rao, A., Luo, C. and Hogan, P.G. (1997) Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol., 15, 707-747.
54. Rooney, J.W., Hodge, M.R., McCaffrey, P.G., Rao, A. and Glimcher, L.H. (1994) A common factor regulates both Th1-and Th2-specific cytokine gene expression. EMBO J., 13, 625-633.
55. Rooney, J.W., Hoey, T. and Glimcher, L.H. (1995) Coordinate and cooperative roles for NF-AT and AP-1 in the regulation of the murine IL-4 gene. Immunity, 2, 473-483.
56. Schreiber, S.L. and Crabtree, G.R. (1992) The mechanism of action of cyclosporin A and FK506. Immunol. Today, 13, 136-142.
57. Schreiber, E., Matthias, P., Muller, M.M. and Schaffner, W. (1989) Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res., 17, 6419.
58. Shaw, K.T.-Y., Ho, A.M., Raghavan, A., Kim, J., Jain, J., Park, J., Sharma, S. and Rao, A. (1995) Immunosuppressive drugs prevent a rapid dephosphorylation of the transcription factor NFAT1 in stimulated immune cells. Proc. Natl Acad. Sci. USA, 92, 11205-11209.
59. Shindo, M., Mullin, G.E., Braun-Elwert, L., Bergasa, N.V., Jones, E.A. and James, S.P. (1996) Cytokine mRNA expression in the liver of patients with primary biliary cirrhosis (PBC) and chronic hepatitis B (CHB). Clin. Exp. Immunol., 105, 254-259.
60. Sigal, N.H. and Dumont, F.J. (1992) Cyclosporin A, FK-506 and rapamycin: pharmacologic probes of lymphocyte signal transduction. Annu. Rev. Immunol., 10, 519-560.
61. Su, F. and Schneider, R.J. (1996) Hepatitis B virus HBx protein activates transcription factor NF-κB by acting on multiple cytoplasmic inhibitors of rel-related proteins. J. Virol., 70, 4558-4566.
62. Tiollais, P., Pourcel, C. and Dejean, A. (1985) The hepatitis B virus. Nature, 317, 489-495.
63. Trede, N.S., Tsytsykova, A.V., Chatila, T., Goldfeld, A.E. and Geha, R.S. (1995) Transcriptional activation of the human TNF-α promoter by superantigen in human monocytic cells. J. Immunol., 155, 902-908.
64. Tsai, E.Y., Yie, J., Thanos, D. and Goldfeld, A.E. (1996) Cell-type-specific regulation of the human tumor necrosis factor-alpha gene in B cells and T cells by NFATp and ATF-2/Jun. Mol. Cell. Biol., 16, 5232-5244.
65. Vassalli, P. (1992) The pathophysiology of tumor necrosis factor. Annu. Rev. Immunol., 10, 411-452.
66. Yao, J., Mackman, N., Edgington, T.S. and Fan, S.-T. (1997) Lipopolysaccharide induction of the tumor necrosis factor-α promoter in human monocytic cells. J. Biol. Chem., 272, 17795-17801.
67. Yen, T.S.B. (1996) Hepadnaviral X protein: review of recent progress. J. Biomed. Sci., 3, 20-30.
68. Yoo, Y.D., Ueda, H., Park, K., Flanders, K.C., Lee, Y.I., Jay, G. and Kim, S.J. (1996) Regulation of transforming growth factor-β1 expression by the hepatitis B virus (HBV) X transactivator. J. Clin. Invest., 97, 388-395.