Proteomic analysis of cellular protein alterations using a hepatitis B virus-producing cellular model

Proteomics

Volumn 8, Issue 10, 2008, Pages 2012-2023

  Tong, Aiping ^a   Wu, Lihong ^a   Lin, Qingsong ^b   Quek, Choon Lau ^c   Zhao, Xia ^a   Li, Jiong ^a   Chen, Ping ^a   Chen, Lijuan ^a   Tang, Hong ^a   Huang, Canhua ^a   Wei, Yu Quan ^a,d  

^a SICHUAN UNIVERSITY   (China)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DEPARTMENT OF ELECTRONICS AND COMPUTER ENGINEERING   (Singapore)

^d SICHUAN UNIVERSITY   (China)

Author keywords

Hepatitis B virus; Hepatocellular carcinoma; HepG2 HepG2.2.15; Two dimensional gel electrophoresis

Indexed keywords

BINDING PROTEIN; CALCIUM ION; CELL PROTEIN; CHAPERONE; MESSENGER RNA; PROTEOME; RETINOL;

ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CLUSTER ANALYSIS; ELECTRON TRANSPORT; HEPATITIS B; HEPATITIS B VIRUS; HOST CELL; HUMAN; IMMUNOREGULATION; LIPID METABOLISM; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; RNA SPLICING; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE; VIRUS REPLICATION;

BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATITIS B VIRUS; HUMANS; LIVER NEOPLASMS; PROTEINS; PROTEOMICS; TANDEM MASS SPECTROMETRY;

HEPATITIS B VIRUS;

EID: 44649161902     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700849     Document Type: Article

References (81)

1. Ganem, D., Prince, A. M., Hepatitis B virus infection-natural history and clinical consequences. N. Engl. J. Med. 2004, 350, 1118-1129.
2. Seeger, C., Mason, W. S., Hepatitis B virus biology. Microbiol. Mol. Biol. Rev. 2000, 64, 51-68.
3. O'Grady, J. G., Smith, H. M., Davies, S. E., Daniels, H. M. et al., Hepatitis B virus reinfection after orthotopic liver transplantation. Serological and clinical implications. J. Hepatol. 1992, 14, 104-111.
4. Marcellin, P., Chang, T., Lim, S. G., Tong, M. J. et al., Adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. N. Engl. J. Med. 2003, 348, 808-816.
5. Aloman, C., Wands, J. R., Resistance of HBV to adefovir dipivoxil: a case for combination antiviral therapy? Hepatology 2003, 38, 1584-1587.
6. Fischer, K. P., Gutfreund, K. S., Tyrrell, D. L., Lamivudine resistance in hepatitis B: mechanisms and clinical implications. Drug Resist. Updat. 2001, 4, 118-128.
7. Delaney, W. E., Locarnini, S., Shaw, T., Resistance of hepatitis B virus to antiviral drugs: current aspects and directions for future investigation. Antivir. Chem. Chemother. 2001, 12, 1-35.
8. Ganem, D., Schneider, R. J., The Molecular Biology of Hepatitis B Viruses, Lippincott, NY 2000.
9. Sun, W., Xing, B., Sun, Y., Du, X. et al., Proteome analysis of hepatocellular carcinoma by two-dimensional difference gel electrophoresis. Mol. Cell. Proteomics 2007 [Epub ahead of print].
10. Kim, M. Y., Park, E., Park, J. H., Park, D. H. et al., Expression profile of nine novel genes differentially expressed in hepatitis B virus-associated hepatocellular carcinomas. Oncogene 2001, 20, 4568-4575.
11. Okabe, H., Satoh, S., Kato, T., Kitahara, O. et al., 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. 2001, 61, 2129-2137.
12. Iizuka, N., Oka, M., Yamada-Okabe, H., Mori, N. et al., Comparison of gene expression profiles between hepatitis B virus- and hepatitis C virus-infected hepatocellular carcinoma by oligonucleotidemicroarray data on the basis of a supervised learning method. Cancer Res. 2002, 62, 3939-3944.
13. Chuma, M., Sakamoto, M., Yamazaki, K., Ohta, T. et al., Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology 2003, 37, 198-207.
14. Lim, S. O., Park, S. J., Kim, W., Park, S. G. et al., Proteome analysis of hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 2002, 291, 1031-1037.
15. Kim, J., Kim, S. H., Lee, S. U., Ha, G. H. et al., Proteome analysis of human liver tumor tissue by two-dimensional gel electrophoresis and matrixassisted laser desorption/ionization-mass spectrometry for identification of disease-related proteins. Electrophoresis 2002, 23, 4142-4156.
16. Li, C., Tan, Y. X., Zhou, H., Ding,S. J. et al., Proteomic analysis of hepatitis B virus-associated hepatocellular carcinoma: Identification of potential tumor markers. Proteomics 2005, 5, 1125-1139.
17. Kim, W., Oe Lim, S., Kim, J. S., Ryu, Y. H. et al., Comparison of proteome between hepatitis B virus- and hepatitis C virus-associated hepatocellular carcinoma. Clin. Cancer Res. 2003, 9, 5493-5500.
18. Hajjou, M., Norel, R., Carver, R., Marion, P. et al., cDNA microarray analysis of HBV transgenic mouse liver identifies genes in lipid biosynthetic and growth control pathways affected by HBV. J. Med. Virol. 2005, 77, 57-65.
19. Zhao, C., Fang, C., Tian, X., Wang, L. et al., Proteomic analysis of hepatitis B surface antigen positive transgenic mouse liver and decrease of cyclophilin A. J. Med. Virol. 2007, 79, 1478-1484.
20. Sells, M. A., Chen, M. L., Acs, G., Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc. Natl. Acad. Sci. USA 1987, 84, 1005-1009.
21. Deres, K., Schroder, C. H., Paessens, A., Goldmann, S. et al., Inhibition of hepatitis B virus replication by drug-induced depletion of nucleocapsids. Science 2003, 299, 893-896.
22. Guo, Y., Guo, H., Zhang, L., Xie, H. et al., Genomic analysis of anti-hepatitis B virus (HBV) activity by small interfering RNA and lamivudine in stable HBV-producing cells. J. Virol. 2005, 79, 14392-14403.
23. Lu, X., Tran, T., Simsek, E., Block, T. M., The alkylated imino sugar, n-(n-Nonyl)-deoxygalactonojirimycin, reduces the amount of hepatitis B virus nucleocapsid in tissue culture. J. Virol. 2003, 77, 11933-11940.
24. Yang, J., Bo, X. C., Ding, X. R., Dai, J. M. et al., Antisense oligonucleotides targeted against asialoglycoprotein receptor 1 block human hepatitis B virus replication. J. Viral Hepat. 2006, 13, 158-165
25. Kabuyama, Y., Resing, K. A., Ahn, N. G., Applying proteomics to signaling networks. Curr. Opin. Genet. Dev. 2004, 14, 492-498.
26. Tong, A., Zhang, H., Li, Z., Gou, L. et al., Proteomic analysis of liver cancer cells treated with suberonylanilide hydroxamic acid. Cancer Chemother. Pharmacol. DOI 10.1007/s00280-007-0536-2.
27. Kawaguchi, R., Yu, J., Honda, J., Hu, J. et al., A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 2007, 315, 820-825
28. Giguere, V., Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocrinol. Rev. 1994, 15, 61-79.
29. Wu, C., Forgues, M., Siddique, S., Farnsworth, J. et al., SAGE transcript profiles of normal primary human hepatocytes expressing oncogenic hepatitis B virus X protein. FASEB J. 2002, 16, 1665-1667.
30. Cui, F., Wang, Y., Wang, J., Wei, K. et al., The up-regulation of proteasome subunits and lysosomal proteases in hepatocellular carcinomas of the HBx gene knockin transgenic mice. Proteomics 2006, 6, 498-504.
31. Bouchard, M. J., Wang, L. H., Schneider, R. J., Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science 2001, 294, 2376-2378.
32. Bouchard, M. J., Schneider, R. J., The enigmatic X gene of hepatitis B virus. J. Virol. 2004, 78, 12725-12734.
33. Zhang, Z., Protzer, U., Hu, Z., Jacob, J., Liang, T. J., Inhibition of cellular proteasome activities enhances hepadnavirus replication in an HBX-dependent manner. J. Virol. 2004, 78, 4566-4572.
34. Hu, Z., Zhang, Z., Kim, J. W., Huang, Y., Liang, T. J., Altered proteolysis and global gene expression in hepatitis B virus X transgenic mouse liver. J. Virol. 2006, 80, 1405-1413
35. Donato, R., Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim. Biophys. Acta 1999, 1450, 191-231.
36. Rogers, J., Calcium-binding proteins: the search for functions. Nature, 1989 339, 661-662.
37. Guignard, F., Mauel, J., Markert, M., Identification and characterization of a novel human neutrophil protein related to the S100 family. Biochem. J. 1995, 309, 395-401.
38. Mueller, A., Bachi, T., Hochli, M., Schafer, B. W., Heizmann, C. W., Subcellular distribution of S100 proteins in tumor cells and their relocation in response to calcium activation. Histochem. Cell. Biol. 1999, 111, 453-459.
39. Choi, Y., Gyoo, P., Sung, Y., Jun-Hi, Jung, G., Calcium ions affect the hepatitis B virus core assembly. Virology 2005, 332, 454-463.
40. Xie, H. Y., Xia, W. L., Zhang, C. C., Wu, L. M. et al., Evaluation of hepatitis B virus replication and proteomic analysis of HepG2.2.15 cell line after cyclosporine A treatment. Acta Pharmacol. Sin. 2007, 28, 975-984.
41. Balmer, J. E., Blomhoff, R., Gene expression regulation by retinoic acid. J. Lipid Res. 2002, 43, 1773-1808.
42. Huan, B., Siddiqui, A., Retinoid X receptor RXR alpha binds to and transactivates the hepatitis B virus enhancer. Proc. Natl. Acad. Sci. USA 1992, 89, 9059-9063.
43. Huan, B., Kosovsky, M. J., Siddiqui, A., Retinoid X receptor alpha transactivates the hepatitis B virus enhancer 1 element by forming a heterodimeric complex with the peroxisome proliferator-activated. J. Virol. 1995, 69, 547-551.
44. Mawson, A. R., Steele, T. A., Possible role of retinoids in hepatitis B virus-associated liver damage. Exp. Biol. Med. 2001, 226, 734-739.
45. Napoli, J. L., Retinoic acid: its biosynthesis and metabolism. Prog. Nucleic Acid Res. Mol. Biol. 1999, 63, 139-188.
46. Farias, E. F., Ong, D. E, Ghyselinck, N. B., Nakajo, S. et al., Cellular retinol-binding protein I, a regulator of breast epithelial retinoic acid receptor activity, cell differentiation, and tumorigenicity. J. Natl. Cancer Inst. 2005, 97, 21-29.
47. Quadro, L., Blaner, W. S., Salchow, D. J., Vogel, S., Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 1999, 18, 4633-4644.
48. Segade, F., Gómez-Márquez, J., Segade, F., Gómez-Márquez, J., Molecules in focus: prothymosin alpha. Int. J. Biochem. Cell. Biol. 1999, 3, 1241-1246.
49. Jiang, X., Kim, H. E., Shu, H., Zhao, Y. et al., Distinctive roles of PHAP proteins and prothymosin-a in a death regulatory pathway. Science 2003, 299, 223-226.
50. Voutsas, I. F., Baxevanis, C. N., Gritzapis, A. D., Missitzis, I., Synergy between interleukin-2 and prothymosin alpha for the increased generation of cytotoxic T lymphocytes against autologous human carcinomas. Cancer Immunol. Immunother. 2000, 49, 449-458.
51. Panneerselvam, C., Haritos, A. A., Caldarella, J., Horecker, B. L, Prothymosin alpha in human blood. Proc. Natl. Acad. Sci. USA 1987, 84, 4465-4469.
52. Franco, F. J., Diaz, C., Barcia, M., Arias, P., et al., Synthesis and apparent secretion of prothymosin alpha by different subpopulations of calf and rat thymocytes. Immunology 1989, 67, 263-268.
53. Mosoian, A., Teixeira, A., High, A. A., Christian, R. E., Novel function of prothymosin alpha as a potent inhibitor of human immunodeficiency virus type 1 gene expression in primary macrophages. J. Virol. 2006, 80, 9200-9206.
54. Melia, T. J., Putting the clamps on membrane fusion: how complexin sets the stage for calcium-mediated exocytosis. FEBS Lett. 2007, 581, 2131-2139.
55. 2+ sensitivity of the fusion process. J. Cell. Sci. 2005, 118, 2239-2246.
56. Watanabe, T., Sorensen, E. M., Naito, A., Schott, M. et al., Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc. Natl. Acad. Sci. USA 2007, 104, 10205-10210.
57. Zhou, T., Evans, A. A., London, W. T., Xia, X. et al., Glutathione S-transferase expression in hepatitis B virus-associated human hepatocellular carcinogenesis. Cancer Res. 1997, 57, 2749-2753.
58. Diamond, D. L., Jacobs, J. M., Paeper, B., Proll, S. C. et al., Proteomic profiling of human liver biopsies: hepatitis C virus-induced fibrosis and mitochondrial dysfunction. Hepatology 2007, 46, 649-657.
59. Adams, J., The proteasome: structure, function, and role in the cell. Cancer Treat. Rev. 2003, 29, 3-9.
60. Kumatori, A., Tanaka, K., Inamura, N., Sone, S. et al., Abnormally high expression of proteasomes in human leukemic cells. Proc. Natl. Acad. Sci. USA 1990, 87, 7071-7075.
61. Kanayama, H., Tanaka, K., Aki, M., Kagawa, S. et al., Changes in expressions of proteasome and ubiquitin genes in human renal cancer cells. Cancer Res. 1991, 51, 6677-6685.
62. Choi, Y. H., Proteasome-mediated degradation of BRCA1 protein in MCF-7 human breast cancer cells. Int. J. Oncol. 2001, 19, 687-693.
63. Milano, A., Iaffaioli, R. V., Caponigro, F., The proteasome: a worthwhile target for the treatment of solid tumours? Eur. J. Cancer 2007, 43, 1125-1133.
64. + T-cell-defined tumor antigen in squamous cell carcinoma of the head and neck. Cancer Res. 2007, 67, 10538-10545.
65. Azuma, K., Sasada, T., Takedatsu, H., Shomura, H. et al., Ran, a small GTPase gene, encodes cytotoxic T lymphocyte (CTL) epitopes capable of inducing HLA-A33-restricted and tumor-reactive CTLs in cancer patients. Clin. Cancer Res. 2004, 10, 6695-6702.
66. + umbilical cord blood hematopoietic stem progenitor cells. Stem Cells Dev. 2005, 14, 188-198.
67. Rice, K. L., Izon, D. J., Ford, J., Boodhoo, A. et al., Overexpression of stem cell associated ALDH1A1, a target of the leukemogenic transcription factor TLX1/HOX11, inhibits lymphopoiesis and promotes myelopoiesis in murine hematopoietic progenitors. Leuk. Res. 2007 [Epub ahead of print].
68. Patel, M., Lu, L., Zander, D. S., Sreerama, L., et al., ALDH1A1 and ALDH3A1 expression in lung cancers: Correlation with histologic type and potential precursors. Lung Cancer 2007 [Epub ahead of print].
69. Weis, K., Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 2003, 112, 441-451.
70. Macara, I., Brownawell, A., Ran, W. K. in: Hall A. (Ed.), GTPases Oxford University Press, Oxford 2000, 198-221
71. Ouellet, V., Guyot, M. C., Le, P. C., Filali-Mouhim, A. et al., Tissue array analysis of expression microarray candidates identifies markers associated with tumor grade and outcome in serous epithelial ovarian cancer. Int. J. Cancer 2006, 119, 599-607.
72. Morgan-Lappe, S. E., Tucker, L. A., Huang, X., Zhang, Q. et al., Identification of Ras-related nuclear protein, targeting protein for xenopus kinesin-like protein 2, and stearoyl-CoA desaturase 1 as promising cancer targets from an RNAi-based screen. Cancer Res. 2007, 67, 4390-4398.
73. Lavia, P., Mileo, A. M., Giordano, A., Paggi, M. G., Emerging roles of DNA tumor viruses in cell proliferation: new insights into genomic instability. Oncogene 2003, 22, 6508-6516.
74. Zhang, X., Zhang, H., Ye, L., Effects of hepatitis B virus X protein on the development of liver cancer. J. Lab. Clin. Med. 2006, 147, 58-66.
75. Wang, X. W., Gibson, M. K., Vermeulen, W., Yeh, H. et al., Abrogation of p53-induced apoptosis by the hepatitis B virus X gene. Cancer Res. 1995, 55, 6012-6016.
76. Elmore, L. W., Hancock, A. R., Chang, S. F., Wang, X. W. et al., Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc. Natl. Acad. Sci. USA 1997, 94, 14707-14712.
77. Shirakata, Y., Kawada, M., Fujiki, Y., Sano, H. et al., The X gene of hepatitis B virus induced growth stimulation and tumorigenic transformation of mouse NIH3T3 cells. Jpn. J. Cancer Res. 1989, 80, 617-621.
78. Terradillos, O., Pollicino, T., Lecoeur, H., Tripodi, M. et al., p53-independent apoptotic effects of the hepatitis B virus HBx protein in vivo and in vitro. Oncogene 1998, 17, 2115-2123.
79. Su, F., Schneider, R. J., Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. USA 1997, 94, 8744-8749.
80. Chirillo, P., Pagano, S., Natoli, G., Puri, P. L. et al., The hepatitis B virus X gene induces p53-mediated programmed cell death. Proc. Natl. Acad. Sci. USA 1997, 94, 8162-8167.
81. Kim, H., Lee, H., Yun, Y., X-gene product of hepatitis B virus induces apoptosis in liver cells. J. Biol. Chem. 1998, 273, 381-385.