Hepatitis B virus X protein differentially effects the ubiquitin-mediated proteasomal degradation of β-catenin depending on the status of cellular p53

Journal of General Virology

Volumn 88, Issue 8, 2007, Pages 2144-2154

  Jung, Jin Kyu ^a   Kwun, Hyun Jin ^a   Lee, Jung Ok ^a   Arora, Payal ^a   Jang, Kyung Lib ^a  

^a Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; HEPATITIS B VIRUS X PROTEIN; PROLINE; PROTEASOME; PROTEIN P53; REGULATOR PROTEIN; SERINE; SEVEN IN ABSENTIA PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE ACTIVATION; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; UPREGULATION;

AMINO ACID SUBSTITUTION; BETA CATENIN; CARCINOMA, HEPATOCELLULAR; CELL LINE; CYTOPLASM; DOWN-REGULATION; GLYCOGEN SYNTHASE KINASE 3; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; VARIATION (GENETICS);

HEPATITIS B VIRUS;

EID: 34547600513     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.82836-0     Document Type: Article

References (56)

1. Aberle, H., Bauer, A., Stappert, J., Kispert, A. & Kemler, R. (1997). β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16, 3797-3804.
2. Ahn, J. Y., Chung, E. Y., Kwun, H. J., Lee, C. W., Sung, Y. C. & Jang, K. L. (2002). Dual effects of hepatitis B virus X protein on the regulation of cell-cycle control depending on the status of cellular p53. J Gen Virol 83, 2765-2772.
3. Albrechtsen, N., Dornreiter, I., Grosse, F., Kim, E., Wiesmuller, L. & Deppert, W. (1999). Maintenance of genomic integrity by p53: complementary roles for activated and non-activated p53. Oncogene 18, 7706-7717.
4. Benn, J., Su, F., Doris, M. & 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.
5. Block T. M., Mehta, A. S., Fimmel, C. J. & Jordan, R. (2003). Molecular viral oncology of hepatocellular carcinoma. Oncogene 22, 5093-5107.
6. Cagatay, T. & Ozturk, M. (2002). p53 mutation as a source of aberrant β-catenin accumulation in cancer cells. Oncogene 21, 7971-7980.
7. Calender, A., Billaud, M., Aubry, J. P., Banchereau, J., Vuillaume, M. & Lenoir, G. M. (1987). Epstein-Barr virus (EBV) induces expression of B-cell activation markers on in vitro infection of EBV-negative B-lymphoma cells. Proc Natl Acad Sci U S A 84, 8060-8064.
8. Cha, M. Y., Kim, C. M., Park Y. M. & Ryu, W. S. (2004). Hepatitis B virus X protein is essential for the activation of Wnt/ β-catenin signaling in hepatoma cells. Hepatology 39, 1683-1693.
9. Ciechanover, A. & Ben-Saadon, R. (2004). N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol 14, 103-106.
10. Colnot S., Decaens, T., Niwa-Kawakita, M., Godard, C., Hamard, G., Kahn, A., Giovannini, M. & Perret, C. (2004). Liver-targeted disruption of Apc in mice activates β-catenin signaling and leads to hepatocellular carcinomas. Proc Natl Acad Sci U S A 101, 17216-17221.
11. Cui, J., Zhou, X., Liu, Y., Tang, Z & Romeih, M. (2003). Wnt signaling in hepatocellular carcinoma: analysis of mutation and expression of β-catenin, T-cell factor-4 and glycogen synthase kinase 3-β genes. J Gastroenterol Hepatol 18, 280-287.
12. de La Coste, A., Romagnolo, B., Billuart, P., Renard, C. A., Buendia, M. A., Soubrane, O., Fabre, M., Chelly, J., Beldjord, C. & other authors (1998). Somatic mutations of the β-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci U S A 95, 8847-8851.
13. Desbois-Mouthon, C., Cadoret, A., Blivet-Van Eggelpoel, M. J., Bertrand, F., Cherqui, G., Perret, C. & Capeau, J. (2001). Insulin and IGF-1 stimulate the β-catenin pathway through two signalling cascades involving GSK-3β inhibition and Ras activation. Oncogene 20, 252-259.
14. Devereux, T. R., Stern, M. C., Flake, G. P., Yu, M. C, Zhang, Z. Q., London, S. J. & Taylor, J. A. (2001). CTNNB1 mutations and β-catenin protein accumulation in human hepatocellular carcinomas associated with high exposure to aflatoxin B1. Mol Carcinog 31, 68-73.
15. Ding, Q., Xia, W., Liu, J. C., Yang, J. Y., Lee, D. F., Xia, J., Bartholomeusz, G., Li, Y., Pan, Y. & other authors (2005). Erk associates with and primes GSK-3β for its inactivation resulting in upregulation of β-catenin. Mol Cell 19, 159-170.
16. Elmore, L. W., Hancock A. R., Chang, S. F., Wang, X. W., Chang, S. Callahan, C. P. Geller, D. A., Will, H. & Harris, C. C. (1997). Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc Natl Acad Sci U S A 94, 14707-14712.
17. Endo, K, Ueda, T., Ueyama, J., Ohta, T. & Terada, T. (2000). Immunoreactive E-cadherin, α-catenin, β-catenin, and γ-catenin proteins in hepatocellular carcinoma: relationships with tumor grade, clinicopathologic parameters, and patients' survival. Hum Pathol 31, 558-565.
18. Everly, D. N., Kusano, S. & Raab-Traub, N. (2004). Accumulation of cytoplasmic β-catenin and nuclear glycogen synthase kinase 3β in Epstein-Barr virus-infected cells. J Virol 78, 11648-11655.
19. Fiucci, G., Beaucourt, S., Duflaut, D., Lespagnol, A., Stumptner-Cuvelette, P., Geant, A., Buchwalter, G., Tuynder, M., Susini, L. & other authors (2004). Siah-1b is a direct transcriptional target of p53: identification of the functional p53 responsive element in the siah-1b promoter. Proc Natl Acad Sci U S A 101, 3510-3515.
20. Gottardi, C. J. & Gumbiner, B. M. (2001). Adhesion signaling: how β-catenin interacts with its partners. Curr Biol 11, R792-R794.
21. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B. & Kinzler, K. W. (1998). Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
22. Holnthoner, W., Pillinger, M., Groger, M., Wolff, K., Ashton, A. W., Albanese, C., Neumeister, P., Pestell, R. G. & Petzelbauer, P. (2002). Fibroblast growth factor-2 induces Lef/Tcf-dependent transcription in human endothelial cells. J Biol Chem 277, 45847-45853.
23. Hu, G. & Fearon, E. R. (1999). Siah-1 N-terminal RING domain is required for proteolysis function, and C-terminal sequences regulate oligomerization and binding to target proteins. Mol Cell Biol 19, 724-732.
24. Iwai, A., Marusawa, H., Matsuzawa, S., Fukushima, T., Hijikata, M., Reed, J. C., Shimotohno, K. & Chiba, T. (2004). Siah-1L, a novel transcript variant belonging to the human Siah family of proteins, regulates β-catenin activity in a p53-dependent manner. Oncogene 23, 7593-7600.
25. Jang, K. L., Shackelford, J., Seo, S. Y. & Pagano, J. S. (2005). Up-regulation of β-catenin by a viral oncogene correlates with inhibition of the seven in absentia homolog 1 in B lymphoma cells. Proc Natl Acad Sci U S A 102, 18431-18436.
26. Janus, F., Albrechtsen, N., Knippschild, U., Wiesmuller, L., Grosse, F. & Deppert, W. (1999). Different regulation of the p53 core domain activities 3′-to-5′ exonuclease and sequence-specific DNA binding. Mol Cell Biol 19, 2155-2168.
27. Jia, L., Wang, X. W. & Harris, C. C. (1999). Hepatitis B virus X protein inhibits nucleotide excision repair. Int J Cancer 80, 875-879.
28. Katoh, H., Shibata, T., Kokubu, A., Ojima, H., Kosuge, T., Kanal, Y. & Hirohashi, S. (2006). Genetic inactivation of the APC gene contributes to the malignant progression of sporadic hepatocellular carcinoma: a case report. Genes Chromosomes Cancer 45, 1050-1057.
29. Kim, C. M., Koike, K., Saito, I., Miyamura, T. & Jay, G. (1991). HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351, 317-320.
30. Kwun, H. J. & Jang, K. L. (2004). Natural variants of hepatitis B virus X protein have differential effects on the expression of cyclin-dependent kinase inhibitor p21 gene. Nucleic Acids Res 32, 2202-2213.
31. Laurent-Puig, P., Legoix, P., Bluteau, O., Belghiti, J., Franco, D., Binot, F., Monges, G., Thomas, G., Bioulac-Sage, P. & Zucman-Rossi, J. (2001). Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis. Gastroenterology 120, 1763-1773.
32. Lee, Y. H. & Yun, Y. (1998). HBx protein of hepatitis B virus activates Jak1-STAT signaling. J Biol Chem 273, 25510-25515.
33. Lee, C. W., Sorensen, T. S., Shikama, N. & La Thangue, N. B. (1998). Functional interplay between p53 and E2F through co-activator p300. Oncogene 16, 2695-2710.
34. Levine, A. J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331.
35. Liu, J., Stevens, J., Rote, C. A., Yost, H. J., Hu, Y., Neufeld, K. L., White, R. L. & Matsunami, N. (2001). Siah-1 mediates a novel β-catenin degradation pathway linking p53 to the adenomatous polyposis coli protein. Mol Cell 7, 927-936.
36. Maguire, H. F., Hoeffler, J. P. & Siddiqui, A. (1991). HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science 252, 842-844.
37. Matsuo, K., Satoh, S., Okabe, H., Nomura, A., Maeda, T., Yamaoka, Y. & Ikai, I. (2003). SIAH1 inactivation correlates with tumor progression in hepatocellular carcinomas. Genes Chromosomes Cancer 36, 283-291.
38. Matsuzawa, S. I. & Reed, J. C. (2001). Siah-1, SIP, and Ebi collaborate in a novel pathway for β-catenin degradation linked to p53 responses. Mol Cell 7, 915-926.
39. Morgan, S. E., Kim, R., Wang, P. C., Bhat, U. G., Kusumoto, H., Lu, T. & Beck, W. T. (2000). Differences in mutant p53 protein stability and functional activity in teniposide-sensitive and -resistant human leukemic CEM cells. Oncogene 19, 5010-5019.
40. Nelson, W. J. & Nusse, R. (2004). Convergence of Wnt, β-catenin, and cadherin pathways. Science 303, 1483-1487.
41. waf1/cip1 and prolongs G1 to S transition via a p53-independent pathway in human hepatoma cells. Oncogene 19, 3384-3394.
42. Paterlini, P., Poussin, K., Kew, M., Franco, D. & Brechot, C. (1995). Selective accumulation of the X transcript of hepatitis B virus in patients negative for hepatitis B surface antigen with hepatocellular carcinoma. Hepatology 21, 313-321.
43. Peifer, M. & Polakis, P. (2000). Wnt signaling in oncogenesis and embryogenesis - a look outside the nucleus. Science 287, 1606-1609.
44. Polakis, P. (2007). The many ways of Wnt in cancer. Curr Opin Genet Dev 17, 45-51.
45. Prost, S., Ford, J. M., Taylor, C., Doig, J. & Harrison, D. J., (1998). Hepatitis B x protein inhibits p53-dependent DNA repair in primary mouse hepatocytes. J Biol Chem 273, 33327-33332.
46. Qadri, I., Maguire, H. F. & Siddiqui, A. (1995). Hepatitis B virus transactivator protein X interacts with the TATA-binding protein. Proc Natl Acad Sci U S A 92, 1003-1007.
47. Sadot, E., Geiger, B., Oren, M. & Ben-Ze'ev, A. (2001). Down-regulation of β-catenin by activated p53. Mol Cell Biol 21, 6768-6781.
48. Satoh, S., Daigo, Y., Furukawa, Y., Kato, T., Miwa, N., Nishiwaki, T., Kawasoe, T., Ishiguro, H., Fujita, M. & other authors (2000). AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat Genet 24, 245-250.
49. Shih, W. L., Kuo, M. L., Chuang, S. E., Cheng, A. L. & Doong, S. L. (2000). Hepatitis B virus X protein inhibits transforming growth factor-β-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J Biol Chem 275, 25858-25864.
50. Siagle, B. L., Lee, T. H., Medina, D., Finegold, M. J. & Butel, J. S. (1996). Increased sensitivity to the hepatocarcinogen diethylnitrosamine in transgenic mice carrying the hepatitis B virus X gene. Mol Carcinog 15, 261-269.
51. Sohn, S., Jaitovitch-Groisman, I., Benlimame, N., Galipeau, J., Batist, G. & Alaoui-Jamali, M. A. (2000). Retroviral expression of the hepatitis B virus x gene promotes liver cell susceptibility to carcinogen-induced site specific mutagenesis. Mutat Res 460, 17-28.
52. Taniguchi, K., Roberts, L. R., Aderca, I. N., Dong, X., Qian, C., Murphy, L. M., Nagomey, D. M., Burgart, L. J., Roche, P. C. & other authors (2002). Mutational spectrum of β-catenin, AXIN1, and AXIN2 in hepatocellular carcinomas and hepatoblastomas. Oncogene 21, 4863-4871.
53. Terradillos, O., Billet, O., Renard, C. A., Levy, R., Molina, T., Briand, P. & Buendia, M. A. (1997). The hepatitis B virus X gene potentiates c-myc-induced liver oncogenesis in transgenic mice. Oncogene 14, 395-404.
54. Tetsu, O. & McCormick F. (1999). β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
55. van de Watering, M., Oosterwegel, M., Dooijes, D. & Clevers, H. (1991). Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J 10, 123-132.
56. Wong, C. M., Fan, S. T. & Ng, I. O. (2001). β-Catenin mutation and overexpression in hepatocellular carcinoma: clinicopathologic and prognostic significance. Cancer 92, 136-145.