Hepatitis B virus HBx protein activates transcription factor NF-κB by acting on multiple cytoplasmic inhibitors of rel-related proteins

Journal of Virology

Volumn 70, Issue 7, 1996, Pages 4558-4566

  Su, Fei ^a   Schneider, Robert J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; DNA BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P105; PROTEIN P50; RAS PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; HEPATITIS B VIRUS; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VIRUS INFECTIVITY; VIRUS TRANSCRIPTION;

EID: 0029982621     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.7.4558-4566.1996     Document Type: Article

References (95)

1. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
2. Arenzana-Seisdedos, F., J. Thompson, M. S. Rodriguez, F. Bachelerie, D. Thomas, and T. T. Hay. 1995. Inducible nuclear expression of newly synthesized IκBα negatively regulates DNA-binding and transcriptional activities of NF-κB. Mol. Cell. Biol. 15:2689-2696.
3. Arima, N., J. A. Molitor, M R. Smith, J. H. Kim, Y. Daitoku, and W. C. Greene. 1991. Human T-cell leukemia type I Tax induces expression of the Rel-related family of κB enhancer-binding proteins: evidence for a pretranslational component of regulation. J. Virol. 65:6892-6899.
4. Auflero, B., and R. J. Schneider. 1990. The hepatitis B virus X-gene product transactivates both RNA polymcrase II and III promoters. EMBO J. 9:497-504.
5. Baeuerle, P. A., and D. Baltimore. 1988. Activation of DNA-binding activity of an apparently cytoplasmic precursor of the NF-κB transcription factor. Cell 53:211-217.
6. Baeuerle, P. A., and D. Baltimore. 1989. The 65-kDa subunit of active NF-κB is required for inhibition of NF-κB by IκB. Genes Dev. 3:1689-1698.
7. Baeuerle, P. A., M. Lenardo, J. W. Pierce, and D. Baltimore. 1988. Phorbol ester induced activation of the NF-κB transcription factor involves dissociation of an apparently cytoplasmic NF-κB/inhibitor complex. Cold Spring Harbor Symp. Quant. Biol. 53:789-798.
8. Beg, A. A., and A. S. Baldwin. 1993. The IκB proteins: mutifunctional regulators of Rel/NF-κB transcription factors. Genes Dev. 7:2064-2070.
9. Beg, A. A., T. S. Finco, P. V. Nantermet, and A. S. Baldwin. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα: a mechanism for NF-κB activation. Mol. Cell. Biol. 13:3301-3310.
10. Beg, A. A., S. M. Ruben, R. I. Scheinman, S. Haskill, C. A. Rosen, and A. S. Baldwin. 1992. IκB intertacts with the nuclear localization sequence of the subunits of NF-κB: a mechanism for cytoplasmic retention. Genes Dev. 6:1899-1913.
11. Benn, J., and R. J. Schneider. 1994. Hepatitis B 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.
12. Benn, J., and R. J. Schneider. 1995. Hepatitis B virus HBx protein deregulates cell cycle checkpoint controls. Proc. Natl. Acad. Sci. USA 92:11215-11219.
13. Benn, J., F. Su, M. Doria, and R. J. Schneider. 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., in press.
14. Beraud, C., S.-C. Sun, P. Ganchi, D. W. Ballard, and W. C. Greene. 1994. Human T-cell leukemia virus type I Tax associates with and is negatively regulated by the NF-κB2 p100 gene product: implications for viral latency. Mol. Cell. Biol. 14:1374-1382.
15. Blank, V., P. Kourilsky, and A. Israel. 1991. Cytoplasmic retention, DNA binding and processing of the NF-κB p50 precursor are controlled by a small region in its C-terminus. EMBO J. 10:4159-4167.
16. Bours, V., J. Villalobos, P. R. Burd, K. Kelly, and U. Siebenlist. 1990. Cloning of a mitogen-inducible gene encoding a κB DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs. Nature (London) 348:76-80.
17. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of a signal response domain in IκBα to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15:2809-2818.
18. Brown, K., S. Park, T. Kanno, G. Franzoso, and I. Siebenlist. 1993 Mutual regulation of the transcriptional activator NF-κB and its inhibitor IκBα. Proc. Natl. Acad. Sci. USA 90:2532-2536.
19. Buehrer, B. N., and R. M. Bell. 1992. Inhibition of sphingosine kinase in vitro and in platelets. J. Biol. Chem. 267:3154-3159.
20. Chen, H., S. Kaneko, R. Girones, R. W. Anderson, W. E. Hornbuckle, B. C. Tennant, P. J. Cote, J. L. Gerin, R. H. Purcell, and R. H. Miller. 1993. The woodchuck hepatitis virus X gene is important for establishment of virus infection in woodchucks. J. Virol. 67:1218-1226.
21. Cheong, J.-H., M.-K. Yi, Y. Lin, and S. Murakami. 1995. Human RPB5, a subunit shared by eukaryotic nuclear polymerases, binds human hepatitis B virus X protein and may play a role in X transactivation. EMBO J. 14:143-150.
22. Chiao, P. J., S. Miyamoto, and I. Verma. 1994. Autoregulation of IκBa activity. Proc. Natl. Acad. Sci. USA 91:28-32.
23. Chirillo, P., M. Falco, P. L. Puri, M. Artini, C. Balsano, M. Levrero, and G. Natoli. 1996. Hepatitis B virus pX activates NF-κB-dependent transcription through a Raf-independent pathway. J. Virol. 70:641-646.
24. Cross, J. C., P. Wen, and W. J. Rutter. 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.
25. Desai, N. N., H. Zhang, A. Olivera, M. E. Mattie, and S. Spiegel. 1992. Sphingosine-1-phosphate, a metabolite of sphingosine, increases phosphatidic acid levels by phospholipase D activation. J. Biol. Chem. 267:23122-23128.
26. Doria, M., N. Klein, R. Lucito, and R. J. Schneider. 1995. Hepatitis B virus HBx protein is a dual specificity cytoplasmic activator of Ras and nuclear activator of transcription factors. EMBO J. 14:4747-4757.
27. Faktor, O., and Y. Shaul. 1990. The identification of hepatitis B virus X gene responsive elements reveals functional similarity of X and HTLV-I tax. Oncogene 5:867-872.
28. Feig, L. A., and G. M. Cooper. 1988. Inhibition of NIH 3T3 cell proliferation by a mutant Ras protein with preferential affinity lor GDP. Mol. Cell. Biol. 8:3235-3243.
29. Finco, T. S., and A. S. Baldwin. 1993. Kappa B site dependent induction of gene expression by diverse inducers of nuclear factor kappa B requires Raf-1. J. Biol. Chem. 268:17676-17679.
30. Finco, T. S., A. A. Beg, and A. S. Baldwin. 1994. Inducible phosphorylation of IκBa is not sufficient for its dissociation from NF-κB and is inhibited by protease inhibitors. Proc. Natl. Acad. Sci. USA 91:11884-11888.
31. Fujimoto, K., H. Yasuda, Y. Sato, and K.-I. Yamamoto. 1995. A role for phosphorylation in the protcolytic processing of the human NF-κB1 precursor. Gene 165:183-189.
32. Ganchi, P. A., S.-C. Sun, W. C. Greene, and D. W. Ballard. 1992. IκB/ MAD-3 masks the nuclear localization signal of NF-κB p65 and acts with the C-terminal activation domain to inhibit NF-κB p65 DNA binding. Mol. Cell. Biol. 3:1339-1352.
33. Ghosh, S., A. M. Gifford, L. R. Riviere, P. Tempst, G. P. Notan, and D. Baltimore. 1990. Cloning of the p50 DNA binding subunit of NF-κB: homology to rel and dorsal. Cell 62:1019-1029.
34. Grilli, M., J. Chiu, and M. Lenardo. 1993. NF-κB and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 143:1-62.
35. Hannun, Y. A. 1994. The sphingomyelin cycle and the second messenger function of ceramide. J. Biol. Chem. 269:3125-3128.
36. Haviv, I., D. Vaizel, and Y. Shaul. 1995. The X protein of hepatitis B virus coactivates potent activation domains. Mol. Cell. Biol. 15:1079-1085.
37. Henkel, T., T. Machleidt, L. Alkalay, M. Kronke, Y. Ben-Neriah, and P. A. Baeuerle. 1993. Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB. Nature (London) 365:182-185.
38. Hohne, M., S. Schaefer, M. Seiler, M. A. Feitelson, D. Paul, and W. H. Gerlich. 1990. Malignant transformation of immortalized transgenic hepatocytes after transfection with hepatitis B virus DNA. EMBO J. 9:1137-1145.
39. Hu, K.-Q., J. M. Vierling, and A. Siddiqui. 1990. Trans-activation of HLA-DR gene by hepatitis B virus X gene product. Proc. Natl. Acad. Sci. USA 87:7140-7144.
40. Kanno, T., K. Brown, G. Franzoso, and U. Siebenlist. 1994. Kinetic analysis of human T-cell leukemia virus type I Tax-mediated activation of NF-κB. Mol. Cell. Biol. 14:6443-6451.
41. Kanno, T., K. Brown, and U. Siebenlist. 1995. Evidence in support of a role for human T-cell leukemia virus type I Tax in activating NF-κB via stimulation of signalling pathways. J. Biol. Chem. 270:11745-11748.
42. Kanno, T., G. Franzoso, and U. Siebenlist. 1994. Human T-cell leukemia virus type I Tax-protein-mediated activation of NF-κB from p100 (NF-κB2)-inhibited cytoplasmic reservoirs. Proc. Natl. Acad. Sci. USA 91:12634-12638.
43. Kaufman, R. J., M. V. Davies, V. K. Pathak, and J. W. B. Hershey. 1989. The phosphorylation state of eukaryotic initiation factor 2 alters translational efficiency of specific mRNAs. Mol. Cell. Biol. 9:946-958.
44. Kaufman, R. J., and P. Muhrta. 1987. Translational control mediated by eucaryotic initiation factor 2 is restricted to specific mRNAs in transfected cells. Mol. Cell. Biol. 7:1568-1571.
45. Kekule, A. S., U. Lauer, L. Weiss, B. Luber, and P. H. Hofschneider. 1993. Hepatitis B virus transactivator HBx uses a tumor promoter signalling pathway. Nature (London) 361:742-745.
46. Kieran, M., V. Blank, F. Logeat, J. Vanderkerckhove, F. Lottspekh, O. Le Bail, M. B. Urban, P. Kourilsky, P. A. Baeuerle, and A. Israel. 1990. The DNA binding subunit of NF-κB is identical to factor KBF1 and homologous to the rel oncogene product. Cell 62:1007-1018.
47. Kim, C.-M., K. Koike, I. Saito, T. Miyamura, and G. Jay. 1991. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature (London) 353:317-320.
48. Koike, K., K. Moriya, S. Iino, H. Yotsuyanagi, Y. Endo, T. Miyamura, and K. Kurokawa. 1994. High-level expression of hepatitis B virus HBx gene and heptocellular carcinogenesis in transgenic mice. Hepatology 19:810-819.
49. Koike, K., K. Moriya, H. Yotsuyanagi, S. Iino, and K. Kurokawa. 1994. Induction of cell cycle progression by hepatitis B virus HBx gene expression in quiescent mouse fibroblasts. J. Clin. Invest. 94:44-49.
50. Kolesnick, R., and D. W. Golde. 1994. The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signalling. Cell 77:325-328.
51. Lacoste, J., L. Petropoulos, N. Pepin, and J. Hiscott. 1995. Constitutive phosphorylation and turnover of IκBα in human T-cell leukemia virus type I-infected and Tax-expressing T cells. J. Virol. 69:564-569.
52. LeBail, O., U. R. Schmidt, and A. Israel. 1993. Promoter analysis of the gene encoding the IκBα/MAD-3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J. 12:5043-5049.
53. Levrero, M., C. Balsano, G. Natoli, M. L. Avantaggiati, and E. Elfassi. 1990. Hepatitis B virus X protein transactivates the long terminal repeals of human immunodeficiency virus types 1 and 2. J. Virol. 64:3082-3086.
54. Li, S., and J. M. Sedivy. 1993. Raf-1 protein kinase activates the NF-κB transcription factor by dissociating the cytoplasmic NF-κB-IκB complex. Proc. Natl. Acad. Sci. USA 90:9247-9251.
55. Liplay, S., R. M. Schmid, E. G. Nabel, and G. J. Nabel. 1994. Transcriptional regulation of NF-κB2: evidence for κB-mediated positive and negative autoregulation. Mol. Cell. Biol. 14:7695-77113.
56. Lucito, R., and R. J. Schneider. 1992. Hepatitis B virus X protein activates transcription factor NF-κB without a requirement for protein kinase C. J. Virol. 66:983-991.
57. Maguire, H. F., J. P. Hoeffler, and A. Siddiqiii. 1991. HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science 252:842-844.
58. Mahe, Y., N. Mukaida, K. Kuno, M. Akiyama, N. Ikeda, K. Matshushima, and S. Murakami. 1991. Hepatitis B virus X protein transactivates human interleukin-8 gene through acting on nuclear factor κB and CCAAT/enhancer -binding protein-like cis elements. J. Biol. Chem. 266:13759-13763.
59. Mercurio, F., J. A. DiDonato, C. Rosette, and M. Karin. 1993. p105 and p98 precursor proteins play an active role in NF-κB mediated signal transduction. Genes Dev. 7:705-718.
60. Meyer, M., W. H. Caselmann, V. Schluler, R. Schreck, P. H. Hofschneider, and P. A. Baeuerle. 1992. Hepatitis B virus transactivator MHBst: activation of NF-κB, selective inhibition by antioxidants and integral membrane localization. EMBO J. 11:2991-3001.
61. Munoz, K., G. Courtois, P. Veschambre, P. Jalinot, and A. Israel. 1994. Tax induces nuclear translocation of NF-κB through dissociation of cytoplasmic complexes containing p105 or p100 hut does not induce degradation of IκBα/MAD3. J. Virol. 68:8035-8044.
62. Natoli, G., M. L. Avantaggiati, P. Chirillo, A. Costanzo, M. Artini, C. Balsano, and M. Levrero. 1994. Induction of the DNA-hinding activity of c-Jun/ c-Fos heterodimers by the hepatitis B virus transactivator pX. Mol. Cell. Biol. 14:989-998.
63. Natoli, G., M. L. Avantaggiati, P. Chirillo, P. L. Puri, A. Ianni, C. Balsano, and M. Levrero. 1994. Ras- and raf-dependent activation of c-jun transcriptional activity by the hepatitis B virus transactivator pX. Oncogene 9:2837-2843.
64. Naumann, M., and C. Scheidereit. 1994. Activation of NF-κB in vivo is regulated hy multiple phosphorylations. EMBO J. 13:4597-4607.
65. Naumann, M., F. G. Wulczyn, and C. Scheidereit. 1993. The NF-κB precursor p105 and the proto-oneogene product Bcl-3 are IκB molecules and control nuclear translocation of NF-κB. EMBO J. 12:213-222.
66. Ohno, H., G. Takimoto, and W. McKeithan. 1990. The candidate protooncogene bcl-3 is related to genes implicated in cell lineage determination and cell cycle control. Cell 60:991-997.
67. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteosome pathway is required for processing the NF-κB1 precursor protein and activation of NF-κB. Cell 78:773-785.
68. Qadri, I., H. F. Maguire, and A. Siddiqui. 1995. Hepatitis B virus transaclivator protein X interacts with the TATA-binding protein. Proc. Natl. Acad. Sci. USA 92:1003-1007.
69. Rice, N. R., M. L. MacKichan, and A. Israel. 1992. The precursor of NF-κB p50 has IκB-like functions. Cell 71:243-253.
70. Ron, D., A. R. Brasier, K. A. Wright, J. E. Tate, and J. F. Habener. 1990. An inducible 50-kDa NF-κB-like protein and a constitutive protein both bind the acute-phase response element of the angiotensinogen gene. Mol. Cell. Biol. 10:1023-1032.
71. Scheinman, R. I., A. A. Beg, and A. S. Baldwin. 1993. NF-κB p100 (Lyt-10) is a component of H2TF1 and can function as an IκB-like molecule. Mol. Cell. Biol. 13:6089-6101.
72. Schutze, S., K. Potthoff, T. Machleidt, D. Berkovic, K. Wiegmann, and M. Kronke. 1992. TNF activates NF-κB by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingmyelin breakdown. Cell 71:765-776.
73. Sen, R., and D. Baltimore. 1986. Inducibility of K immunoglobulin enhancer binding protein NF-κB by a posttranslational mechanism. Cell 47:921-928.
74. Seto, E., P. J. Mitchell, and T. S. B. Yen. 1990. Transactivation by the hepatitis B virus X protein depends on AP-2 and other transcription factors. Nature (London) 344:72-74.
75. Seto, E., T. S. B. Yen, B. M. Peterlin, and J.-H. Ou. 1988. Trans-activation of the human immunodeficiency virus long terminal repeat by the hepatitis B virus X protein. Proc. Natl. Acad. Sci. USA 85:8290-8286.
76. Siddiqui, A., R. Gaynor, A. Srinivasan, J. Mapoles, and R. W. Farr. 1989. Trans-activation of viral enhancers including long terminal repeat of the human immunodeficiency virus by the hepatitis B virus X protein. Virology 169:474-484.
77. Suchi, M., T. Dinur, R. J. Desnick, S. Gatl, L. Pereira, E. Gilboa, and E. H. Schuchman. 1992. Retroviral-mediated transfer of the human acid sphingomyelinase cDNA: correction of the metabolic defect in cultured Niemann-Pick disease cells. Proc. Natl. Acad. Sci. USA 89:3227-3231.
78. Sun, S., P. A. Ganchi, D. W. Ballard, and W. C. Grecne. 1993. NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 259:1912-1915.
79. Sun, S.-C., J. Elwood, C. Beraud, and W. C. Greene. 1994. Human T-cell leukemia virus type I Tax activation of NF-κB/Rel involves phosphorylation and degradation of IκBα and RelA (p65)-mediated induction of the c-rel gene. Mol. Cell. Biol. 14:7377-7384.
80. Sun, S.-C., P. A. Ganchi, C. Beraud, D. W. Ballard, and W. C. Greene. 1994. Autoregulation of the NF-κB transactivator RelA (p65) by multiple cytoplasmic inhibitors containing ankyrin motifs. Proc. Natl. Acad. Sci. USA 91:1346-13511.
81. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
82. Traenckner, E. B.-M., S. Wilk, and P. A. Baeuerle. 1994. A proteosome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylaled form of IκBα that is still bound to NF-κB. EMBO J. 13:5433-5441.
83. Twu, J.-S., M.-Y. Lai, D.-S. Chen, and W. S. Robinson. 1993. Activation of protooncogene c-jun by the X protein of hepatitis B virus. Virology 192:346-350.
84. Twu, J.-S., and W. S. Robinson. 1989. Hepatitis B virus X gene can transactivate heterologous viral sequences. Proc. Natl. Acad. Sci. USA 86:2046-2050.
85. Twu, J. S., and R. H. Schloemer. 1987. Transcriptional trans-activating function of hepatitis B virus. J. Virol. 61:3448-3453.
86. Unger, T., and Y. Shaul. 1990. The X protein of the hepatitis B virus acts as a transcription factor when targeted to its responsive element. EMBO J. 9:1889-1895.
87. Wang, H.-D., C.-H. Yuh, C. V. Dang, and D. L. Johnson. 1995. The hepatitis B virus X protein increases the cellular level of TATA-binding protein which mediates transactivation of RNA polymerase III genes. Mol. Cell. Biol. 15:6720-6728.
88. Watanabe, M., M.-A. Muramatsu, H. Hirai, T. Suzuki, J. Fujisawa, M. Yoshida, K.-I. Arai, and N. Arai. 1993. HTLV-1 encoded Tax in association with NF-κB precursor p105 enhances nuclear localization of NF-κB p50 and p65 in transfectcd cells. Oncogene 8:2949-2958.
89. Williams, J. S., and O. M. Andrisani. 1995. The hepatitis B virus X protein targets the basic region-leucine zipper domain of CREB. Proc. Natl. Acad. Sci. USA 92:3819-3823.
90. Wolf, R. A., R. T. Dobrowsky, A. Bielawska, L. M. Obeid, and Y. A. Hannun. 1994. Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem. 269:19605-19609.
91. Yoshimura, K., M. A. Rosenfeld, P. Seth, and R. G. Crystal. 1993. Adenovirus-mediated augmentation of cell transfection with unmodified plasmid vectors. J. Biol. Chem. 268:2300-2303.
92. Zabel, U., and P. A. Baeuerle. 1990. Purified human IκB can rapidly dissociate the complex of the NF-κB transcription factor with its cognate DNA. Cell 61:255-265.
93. Zahm, P., P. H. Hofschneider, and R. Koshy. 1988. The HBV X-ORF encodes a transactivator: a potential factor in viral hepatocarcinogenesis. Oncogene 3:169-177.
94. Zhou, D.-X., A. Taraboulous, J.-H. Ou, and T. S. B. Yen. 1990. Activation of class I major histocompatibility complex gene expression by hepatitis B virus. J. Virol. 64:4025-4028.
95. Zoulim, F., J. Saputelli, and C. Seeger. 1994. Woodchuck hepatitis virus X protein is required for viral infection in vivo. J. Virol. 68:2026-2030.