Activation of Src family kinases by hepatitis B virus HBx protein and coupled signaling to Ras

Molecular and Cellular Biology

Volumn 17, Issue 11, 1997, Pages 6427-6436

  Klein, Nicola P ^a   Schneider, Robert J ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; RAF PROTEIN; RAS PROTEIN; TRANSCRIPTION FACTOR AP 1; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VIRUS REPLICATION;

EID: 0030764344     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.11.6427     Document Type: Article

References (75)

1. Aronheim, A., D. Engelberg, N. Li, N. Al-Alawi, J. Schlessinger, and M. Karin. 1994. Membrane targeting of the nucleotidc exchange factor Sos is sufficient for activating the Ras signaling pathway. Cell 78:949-961.
2. Aufiero, B., and R. J. Schneider. 1990. The hepatitis B virus X-gene product trans-activates both RNA polymerase II and III promoters. EMBO J. 9:497-504.
3. Balsano, C., M. L. Avantaggiati, G. Natoli, E. DeMarzio, H. Will, M. Perricaudet and M. Levrero. 1991. Full-length and truncated versions of the hepatitis B virus (HBV) X protein (pX) transactivate the c-myc proto-oncogene at the transcriptional level. Biochem. Biophys. Res. Commun. 176. 985-992.
4. Beasley, R. P., L. Y. Hwang, C. C. Lin, and C. S. Chien. 1981. Hepatocellular carcinomas and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet ii: 1129-1133.
5. 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.
6. 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.
7. Benn, J., F. Su, M. Doria, and R. J. Schneider. 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.
8. Blum, H. E., Z.-S. Zhang, E. Galun, F. von Weizsäcker, B. Garner, T. J. Liang, and J. R. Wands. 1992. Hepatitis B virus X protein is not central to the viral life cycle in vitro. J. Virol. 66:1223-1227.
9. Boguski, M. S., and F. McCormick. 1993. Proteins regulating Ras and its relatives. Nature (London) 366:643-653.
10. ras in fibroblasts. Mol. Cell. Biol. 13:1903-1910.
11. Butel, J. S., T.-H. Lee, and B. L. Slagle. 1996. Is the DNA repair system involved in hepatitis B virus mediated hepatocellular carcinogenesis? Trends Microbiol. 4:119-124.
12. 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.
13. 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.
14. Chisari, F. V., and C. Ferrari. 1995. Hepatitis B virus immunopathogenesis. Annu. Rev. Immunol. 13:29-60.
15. Courtneidge, S. A. 1985. Activation of the pp60c-src kinase by middle T antigen binding or by dephosphorylation. EMBO J. 4:1471-1477.
16. Courtneidge, S. A., R. Dhand, D. Pilat, G. M. Twamley, M. D. Waterfield, and M. Roussel. 1993. Activation of Src family kinases by colony stimulating factor-1, and their association with its receptor. EMBO J. 12:943-950.
17. Courtneidge, S. A., and A. E. Smith. 1983. Polyoma virus transforming protein associates with the product of the c-src cellular gene. Nature (London) 303:435-439.
18. 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.
19. Dandri, M., P. Schirmacher, and C. E. Rogler. 1996. Woodchuck hepatitis virus X protein is present in chronically infected woodchuck liver and wood-chuck hepatocellular carcinomas which are permissive for viral replication. J. Virol. 70:5246-5254.
20. Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature (London) 383:547-550.
21. Dilworth, S. M., C. E. P. Brewster, M. D. Jones, L. Lanfrancone, G. Pelicci, and P. G. Pelicci. 1994. Transformation by polyoma virus middle T-antigen involves the binding and tyrosine phosphorylation of She. Nature (London) 367:87-90.
22. 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.
23. Downward, J., J. D. Graves, P. H. Warne, S. Rayter, and D. A. Cantrell. 1990. Stimulation of p21Ras upon T-cell activation. Nature (London) 346:719.
24. Erpel, T., and S. A. Courtneidge. 1995. Src family protein tyrosine kinases and cellular signal transduction pathways. Curr. Opin. Cell Biol. 7:176-182.
25. Ganem, D., and H. E. Varmus. 1987. The molecular biology of the hepatitis B viruses. Annu. Rev. Biochem. 56:651-693.
26. Haviv, I., D. Vaizel, and Y. Shaul. 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., D. Vaizel, and Y. Shaul. 1995. The X protein of hepatitis B virus coactivates potent activation domains. Mol. Cell. Biol. 15:1079-1085.
28. Huang, J., J. Kwong, E. C.-Y. Sun, and T. J. Liang. 1996. Proteasome complex as a potential cellular target of hepatitis B virus X protein. J. Virol. 70:5582-5591.
29. Kaplan, K. B., J. R. Swedlow, D. O. Morgan, and H. E. Varmus. 1995. c-Src enhances the spreading of src-/-fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9:1505-1517.
30. 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.
31. 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.
32. Klein, N., and R. J. Schneider. An essential role for Src activation by the HBx protein in HBV replication. Submitted for publication.
33. 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.
34. Koike, K., K. Moriya, H. Yotsuyanagi, S. lino, 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.
35. Lee, T.-H., S. J. Elledge, and J. S. Butel. 1995. Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. J. Virol. 69:1107-1114.
36. Lee, T.-H., M. J. Finegold, R. F. Shen, J. L. DeMayo, S. L. C. Woo, and J. S. Butel. 1990. Hepatitis B virus transactivator X protein is not tumorigenic in transgenic mice. J. Virol. 64:5939-5947.
37. 2+-induced regulation of ion channel and MAP kinase functions. Nature (London) 376:737-745.
38. Levrero, M., C. Balsano, G. Natoli, M. L. Avantaggiati, and E. Elfassi. 1990. Hepatitis B virus X protein transactivates the long terminal repeats of human immunodeficiency virus types 1 and 2. J. Virol. 64:3082-3086.
39. Levrero, M., O. Jean-Jean, C. Balsano, H. Wills, and M. Perricaudet. 1990. Hepatitis B virus (HBV) X gene expression in human cells and anti-HBx antibodies detection in chronic HBV infection. Virology 174:299-304.
40. Li, B., D. Kaplan, H. Kung, and T. Kamata. 1992. Nerve growth factor stimulation of the Ras-guanine nucleotide exchange factor and GAP activities. Science 256:1456-1459.
41. Li, N., A. Batzer, R. Daly, V. Yajnik, E. Skolnick, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine-nucleotide-releasing factor hSosl binds to Grb2 and links receptor tyrosine kinases to Ras signaling. Nature (London) 363:85-87.
42. Lowell, C. A., and P. Soriano. 1996. Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev. 10:1845-1857.
43. Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, D. Bar-Sagi, and J, Schlessinger. 1992. The SH2 and SH3 domain-containing protein Grb2 links receptor tyrosine kinases to Ras signaling. Cell 70:431-442.
44. 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.
45. Luttrell, L. M., B. E. Hawes, T. V. Biesen, D. K. Luttrell, T. J. Lansing, and R. J. Lefkowitz. 1996. Role of c-Src tyrosine kinase in G protein-coupled receptor-and GB-γ subunit-mediated activation of mitogen-activated protein kinases. J. Biol. Chem. 271:19443-19450.
46. Maguire, H. F., J. P. Hoeffler, and A. Siddiqui. 1991. HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science 252:842-844.
47. Messerschmitt, A. S., N. Dunant, and K. Balmmer-Hofer. 1997. DNA tumor viruses and Src family tyrosine kinases, an intimate relationship. Virology 227:271-280.
48. ras · GMPPNP is dependent on B-Raf. Mol. Cell. Biol. 14: 7153-7162.
49. Natoli, G., M. L. Avantaggiati, P. Chirillo, A. Costanzo, M. Artini, C. Balsano, and M. Levrero. 1994. 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.
50. 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.
51. Pellici, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P. G. Pellici. 1992. A novel transforming protein (She) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
52. Pruett, W., Y. E. Rose, A. G. Batzer, N. Harada, and E. Y. Skolnick. 1995. Association between GRB2/Sos and insulin receptor substrate 1 is not sufficient for activation of extracellular signal-regulated kinases by interleukin-4: implication for Ras activation by insulin. Mol. Cell. Biol. 15:1778-1785.
53. Qadri, I., H. F. Maguire, and A. Siddiqui. 1995. Hepatitis B virus transactivator protein X interacts with the TATA-binding protein. Proc. Natl. Acad. Sci. USA 92:1003-1007.
54. Rosen, L. B., D. D. Ginty, M. J. Weber, and M. E. Greenberg. 1994. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12:1207-1221.
55. Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P. G. Pellici, J. Schlessinger, and T. Pawson. 1992. Association of the She and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature (London) 360:689-692.
56. Rusanescu, G., H. Qi, S. M. Thomas, J. S. Brugge, and S. Halegoua. 1995. Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron 15:1415-1425.
57. Schek, N., R. Bartenschlager, C. Kuhn, and H. Schaller. 1991. Phosphorylation and rapid turnover of hepatitis B virus X protein expressed in HepG2 cells from a recombinant vaccinia virus. Oncogene 6:1735-1744.
58. Schneider, R. J. 1996. Adenovirus and vaccinia virus translational control, p. 575-605. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. 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.
60. Slagle, B. L., T. H. Lee, D. Medina, M. J. Finegold, and J. S. Butel. 1996. Increased sensitivity to the hepatocarcinogen diethylnitrosamine in transgenic mice carrying the hepatitis B virus X gene. Mol. Carcinog. 15:261-269.
61. Songyang, Z., et al. 1993. SH2 domains recognize specific phosphorylation sequences. Cell 72:767-778.
62. Spandau, D. F., and C. H. Lee. 1988. trans-activation of viral enhancers by the hepatitis B virus X protein. J. Virol. 62:427-434.
63. Su, F., and R. J. Schneider. 1996. HBV HBx protein activates transcription factor NF-κB by acting on multiple cytoplasmic inhibitors of Rel-related proteins. J. Virol. 70:4558-4566.
64. Su, F., and R. J. Schneider. 1997. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor α. Proc. Natl. Acad. Sci. USA 94:8744-8749.
65. Truant, R., J. Antunovic, J. Greenblatt, C. Prives, and J. A. Cromlish. 1995. Direct interaction of the hepatitis B virus HBx protein with p53 leads to inhibition by HBx of p53 response element-directed transactivation. J. Virol. 69:1851-1859.
66. 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.
67. 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-hinding protein which mediates transactivation of RNA polymerase III genes. Mol. Cell. Biol. 15: 6720-6728.
68. Wang, X. W., K. Forrester, H. Yeh, M. A. Feitelson, J. Gu, and C. C. Harris. 1994. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding transcriptional activity, and association with transcription factor ERCC3. Proc. Natl. Acad. Sci. USA 91:2230-2234.
69. 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.
70. Yen, T. S. B. 1996. Hepadnaviral X protein: review of recent progress. J. Biomed. Sci. 3:20-30.
71. Yueh, A., and R. J. Schneider. 1996. Selective translation by ribosome jumpini: in adenovirus infected and heat shocked cells. Genes Dev. 10:1557-1567.
72. Zentgraf, H., G. Herrmann, R. Klein, P. Schranz, I. Loncarevic, D. Herrmann, K. Hubner, and C. H. Schroder. 1990. Mouse monoclonal antibody against hepatitis B virus X protein synthesized in Escherichia coli: detection of reactive antigen in liver cell carcinoma and chronic hepatitis. Oncology 47:143-148.
73. Zhang, K., A. G. Papageorge, and D. R. Lowy. 1992. Mechanistic aspects of signaling through Ras in NIH 3T3 cells. Science 257:671-674.
74. Zheng, Y.-X., J. Riegler, J. Wu, and T. S. B. Yen. 1994. Novel short transcripts of hepatis B virus X gene derived from intragenic promoter. J. Biol. Chem. 269:22593-22598.
75. 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.