The HBx protein of hepatitis B virus regulates the expression, intracellular distribution and functions of ribosomal protein S27a

Journal of General Virology

Volumn 93, Issue 4, 2012, Pages 706-715

  Fatima, Grace ^a   Mathan, Ganeshan ^b   Kumar, Vijay ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^b BHARATHIDASAN UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINAL EXTENSION PROTEIN; COMPLEMENTARY DNA; HEPATITIS B VIRUS X PROTEIN; HYBRID PROTEIN; PROTEIN; RIBOSOMAL PROTEIN S27A; RIBOSOME PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LYSOSOME; MOUSE; NONHUMAN; NUCLEOLUS; ONCOGENE MYC; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RESPIRATORY CHAIN; RNA INTERFERENCE; UPREGULATION; VIRUS CARCINOGENESIS;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; HEPATITIS B VIRUS; HUMANS; LIVER; LIVER NEOPLASMS; MICE; MICE, TRANSGENIC; RIBOSOMAL PROTEINS; TRANS-ACTIVATORS;

HEPATITIS B VIRUS; MUS;

EID: 84858175912     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.035691-0     Document Type: Article

References (58)

1. Adams, S. M., Sharp, M. G., Walker, R. A., Brammar, W. J. & Varley, J. M. (1992). Differential expression of translation-associated genes in benign and malignant human breast tumours. Br J Cancer 65, 65-71.
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
3. Amsterdam, A., Sadler, K. C., Lai, K., Farrington, S., Bronson, R. T., Lees, J. A. & Hopkins, N. (2004). Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2, e139.
4. Benhenda, S., Cougot, D., Buendia, M. A. & Neuveut, C. (2009). Hepatitis B virus X protein molecular functions and its role in virus life cycle and pathogenesis. Adv Cancer Res 103, 75-109.
5. Benn, J., Su, F., Doria, 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 rotein kinases. J Virol 70, 4978-4985.
6. Bocquel, M. T., Kumar, V., Stricker, C., Chambon, P. & Gronemeyer, H. (1989). The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cellspecific. Nucleic Acids Res 17, 2581-2595.
7. Bouchard, M. J. & Schneider, R. J. (2004). The enigmatic X gene of hepatitis B virus. J Virol 78, 12725-12734.
8. Bratthauer, G. L. (1994). The avidin-biotin complex (ABC) method. Methods Mol Biol 34, 175-184.
9. Caselmann, W. H. (1996). Trans-activation of cellular genes by hepatitis B virus proteins: a possible mechanism of hepatocarcinogenesis. Adv Virus Res 47, 253-302.
10. Chemin, I. & Zoulim, F. (2009). Hepatitis B virus induced hepatocellular carcinoma. Cancer Lett 286, 52-59.
11. Chen, X., Cheung, S. T., So, S., Fan, S. T., Barry, C., Higgins, J., Lai, K. M., Ji, J., Dudoit, S. & other authors (2002). Gene expression patterns in human liver cancers. Mol Biol Cell 13, 1929-1939.
12. Choedon, T., Shukla, S. K. & Kumar, V. (2010). Chemopreventive and anti-cancer properties of the aqueous extract of flowers of Butea monosperma. J Ethnopharmacol 129, 208-213.
13. Echave, P., Conlon, I. J. & Lloyd, A. C. (2007). Cell size regulation in mammalian cells. Cell Cycle 6, 218-224.
14. Finley, D., Bartel, B. & Varshavsky, A. (1989). The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338, 394-401.
15. Fourel, G., Trepo, C., Bougueleret, L., Henglein, B., Ponzetto, A., Tiollais, P. & Buendia, M. A. (1990). Frequent activation of N-myc genes by hepadnavirus insertion in woodchuck liver tumours. Nature 347, 294-298.
16. Ghetti, A., Piñol-Roma, S., Michael, W. M., Morandi, C. & Dreyfuss, G. (1992). hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res 20, 3671-3678.
17. Graveel, C. R., Jatkoe, T., Madore, S. J., Holt, A. L. & Farnham, P. J. (2001). Expression profiling and identification of novel genes in hepatocellular carcinomas. Oncogene 20, 2704-2712.
18. Henkler, F., Hoare, J., Waseem, N., Goldin, R. D., McGarvey, M. J., Koshy, R. & King, I. A. (2001). Intracellular localization of the hepatitis B virus HBx protein. J Gen Virol 82, 871-882.
19. Höhne, M., Schaefer, S., Seifer, M., Feitelson, M. A., Paul, D. & Gerlich, W. H. (1990). Malignant transformation of immortalized transgenic hepatocytes after transfection with hepatitis B virus DNA. EMBO J 9, 1137-1145.
20. Hu, Z., Zhang, Z., Doo, E., Coux, O., Goldberg, A. L. & Liang, T. J. (1999). Hepatitis B virus X protein is both a substrate and a potential inhibitor of the proteasome complex. J Virol 73, 7231-7240.
21. Johnston, G. C., Pringle, J. R. & Hartwell, L. H. (1977). Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res 105, 79-98.
22. Jorgensen, P., Rupes, I., Sharom, J. R., Schneper, L., Broach, J. R. & Tyers, M. (2004). A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 18, 2491-2505.
23. Kanayama, H., Tanaka, K., Aki, M., Kagawa, S., Miyaji, H., Satoh, M., Okada, F., Sato, S., Shimbara, N. & Ichihara, A. (1991). Changes in expressions of proteasome and ubiquitin genes in human renal cancer cells. Cancer Res 51, 6677-6685.
24. Khattar, E. & Kumar, V. (2010). Mitogenic regulation of p27(Kip1) gene is mediated by AP-1 transcription factors. J Biol Chem 285, 4554-4561.
25. Kim, D. G. (2006). Differentially expressed genes associated with hepatitis B virus HBx and MHBs protein function in hepatocellular carcinoma. Methods Mol Biol 317, 141-155.
26. Kim, M. Y., Park, E., Park, J. H., Park, D. H., Moon, W. S., Cho, B. H., Shin, H. S. & Kim, D. G. (2001). Expression profile of nine novel genes differentially expressed in hepatitis B virus-associated hepatocellular carcinomas. Oncogene 20, 4568-4575.
27. Kim, J. H., You, K. R., Kim, I. H., Cho, B. H., Kim, C. Y. & Kim, D. G. (2004). Over-expression of the ribosomal protein L36a gene is associated with cellular proliferation in hepatocellular carcinoma. Hepatology 39, 129-138.
28. Kremsdorf, D., Soussan, P., Paterlini-Brechot, P. & Brechot, C. (2006). Hepatitis B virus-related hepatocellular carcinoma: paradigms for viral-related human carcinogenesis. Oncogene 25, 3823-3833.
29. Kumar, V. (2008). Animal models of hepatitis B-related hepatocellular carcinoma in cancer research. In The Pleitropic Functions of the Viral Protein HBx in Hepatitis B Virus Infection and Development of Liver Cancer, pp. 179-194. Edited by J. Kobarg. Trivandrum, India: Research Signpost.
30. Kumar, V. & Sarkar, D. P. (2004). Hepatitis B virus X protein (HBx): structure-function relationships and role in viral pathogenesis. In Handbook of Experimental Pharmacology, vol. 166, pp. 377-407. Edited by S. J. Triezenberg, J. Kaufman & M. Gossen. Germany: Springer.
31. Kumar, V., Jayasuryan, N. & Kumar, R. (1996). A truncated mutant (residues 58-140) of the hepatitis B virus X protein retains transactivation function. Proc Natl Acad Sci U S A 93, 5647-5652.
32. Lian, Z., Pan, J., Liu, J., Zhang, S., Zhu, M., Arbuthnot, P., Kew, M. & Feitelson, M. A. (1999). The translation initiation factor, hu-Sui1 may be a target of hepatitis B X antigen in hepatocarcinogenesis. Oncogene 18, 1677-1687.
33. Masucci, M. G. (2004). Epstein-Barr virus oncogenesis and the ubiquitin-proteasome system. Oncogene 23, 2107-2115.
34. Mathan, G., Fatima, G., Saxena, A. K., Chandan, B. K., Jaggi, B. S., Gupta, B. D., Qazi, G. N., Balasundaram, C., Anand Rajan, K. D. & other authors (2011). Chemoprevention with aqueous extract of Butea monosperma flowers results in normalization of nuclear morphometry and inhibition of a proliferation marker in liver tumors. Phytother Res 25, 324-328.
35. McMahon, B. J. (2009). The natural history of chronic hepatitis B virus infection. Hepatology 49 (Suppl.), S45-S55.
36. Monia, B. P., Ecker, D. J., Jonnalagadda, S., Marsh, J., Gotlib, L., Butt, T. R. & Crooke, S. T. (1989). Gene synthesis, expression, and processing of human ubiquitin carboxyl extension proteins. J Biol Chem 264, 4093-4103.
37. Monia, B. P., Ecker, D. J., Finley, D. & Crooke, S. T. (1990). A human ubiquitin carboxyl extension protein functions in yeast. J Biol Chem 265, 19356-19361.
38. Mukherji, A., Janbandhu, V. C. & Kumar, V. (2007). HBx-dependent cell cycle deregulation involves interaction with cyclin E/A-cdk2 complex and destabilization of p27Kip1. Biochem J 401, 247-256.
39. Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T. & Sato, J. (1982). Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42, 3858-3863.
40. Neufeld, T. P. & Edgar, B. A. (1998). Connections between growth and the cell cycle. Curr Opin Cell Biol 10, 784-790.
41. Nijhara, R., Jana, S. S., Goswami, S. K., Rana, A. K., Majumdar, S. S., Kumar, V. & Sarkar, D. P. (2001). Sustained activation of mitogenactivated protein kinases and activator protein 1 by the hepatitis B virus X protein in mouse hepatocytes in vivo. J Virol 75, 10348-10358.
42. Okabe, H., Satoh, S., Kato, T., Kitahara, O., Yanagawa, R., Yamaoka, Y., Tsunoda, T., Furukawa, Y. & Nakamura, Y. (2001). Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res 61, 2129-2137.
43. Piper, R. C. & Luzio, J. P. (2007). Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr Opin Cell Biol 19, 459-465.
44. Redman, K. L. & Rechsteiner, M. (1988). Extended reading frame of a ubiquitin gene encodes a stable, conserved, basic protein. J Biol Chem 263, 4926-4931.
45. Redman, K. L. & Rechsteiner, M. (1989). Identification of the long ubiquitin extension as ribosomal protein S27a. Nature 338, 438-440.
46. Schmittgen, T. D. & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3, 1101-1108.
47. Shirakata, Y., Kawada, M., Fujiki, Y., Sano, H., Oda, M., Yaginuma, K., Kobayashi, M. & Koike, K. (1989). The X gene of hepatitis B virus induced growth stimulation and tumorigenic transformation of mouse NIH3T3 cells. Jpn J Cancer Res 80, 617-621.
48. Shirota, Y., Kaneko, S., Honda, M., Kawai, H. F. & Kobayashi, K. (2001). Identification of differentially expressed genes in hepatocellular carcinoma with cDNA microarrays. Hepatology 33, 832-840.
49. Ueda, H., Ullrich, S. J., Gangemi, J. D., Kappel, C. A., Ngo, L., Feitelson, M. A. & Jay, G. (1995). Functional inactivation but not structural mutation of p53 causes liver cancer. Nat Genet 9, 41-47.
50. Wang, X. W., Forrester, K., Yeh, H., Feitelson, M. A., Gu, J. R. & Harris, C. C. (1994). Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc Natl Acad Sci U S A 91, 2230-2234.
51. Wang, C., Politz, J. C., Pederson, T. & Huang, S. (2003). RNA polymerase III transcripts and the PTB protein are essential for the integrity of the perinucleolar compartment. Mol Biol Cell 14, 2425-2435.
52. Warner, J. R. & McIntosh, K. B. (2009). How common are extraribosomal functions of ribosomal proteins? Mol Cell 34, 3-11.
53. Wong, J. M., Mafune, K., Yow, H., Rivers, E. N., Ravikumar, T. S., Steele, G. D., Jr & Chen, L. B. (1993). Ubiquitin-ribosomal protein S27a gene overexpressed in human colorectal carcinoma is an early growth response gene. Cancer Res 53, 1916-1920.
54. Wool, I. G. (1996). Extraribosomal functions of ribosomal proteins. Trends Biochem Sci 21, 164-165.
55. Xu, L., Hui, L., Wang, S., Gong, J., Jin, Y., Wang, Y., Ji, Y., Wu, X., Han, Z. & Hu, G. (2001a). Expression profiling suggested a regulatory role of liver-enriched transcription factors in human hepatocellular carcinoma. Cancer Res 61, 3176-3181.
56. Xu, X. R., Huang, J., Xu, Z. G., Qian, B. Z., Zhu, Z. D., Yan, Q., Cai, T., Zhang, X., Xiao, H. S. &other authors (2001b). Insight into hepatocellular carcinogenesis at transcriptome level by comparing gene expression profiles of hepatocellular carcinoma with those of corresponding noncancerous liver. Proc Natl Acad Sci U S A 98, 15089-15094.
57. Yamamoto, T. (2000). Molecular mechanism of monocyte predominant infiltration in chronic inflammation: mediation by a novel monocyte chemotactic factor, S19 ribosomal protein dimer. Pathol Int 50, 863-871.
58. Yang, J. D. & Roberts, L. R. (2010). Hepatocellular carcinoma: a global view. Nat Rev Gastroenterol Hepatol 7, 448-458.