Hepatitis B virus X protein impairs hepatic insulin signaling through degradation of IRS1 and induction of SOCS3

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Kim, KyeongJin ^a   Kim, Kook Hwan ^a   Cheong, JaeHun ^a  

^a Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B VIRUS X PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; IRS1 PROTEIN, MOUSE; PROTEASOME; SOCS3 PROTEIN, HUMAN; SOCS3 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING; TRANSACTIVATOR PROTEIN;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; HUMAN; LIVER CELL CARCINOMA; METABOLISM; MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICE; MICE, TRANSGENIC; PROTEASOME ENDOPEPTIDASE COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATORS;

EID: 77957959354     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008649     Document Type: Article

References (51)

1. Lee WM (1997) Hepatitis B virus infection. N Engl J Med 337: 1733-1745.
2. Lok AS, McMahon BJ (2007) Chronic hepatitis B. Hepatology 45: 507-539.
3. Murakami S (1999) Hepatitis B virus X protein: structure, function and biology. Intervirology 42: 81-99.
4. Tang H, Oishi N, Kaneko S, Murakami S (2006) Molecular functions and biological roles of hepatitis B virus x protein. Cancer Sci 97: 977-983.
5. Hajjou M, Norel R, Carver R, Marion P, Cullen J, et al. (2005) cDNA microarray analysis of HBV transgenic mouse liver identifies genes in lipid biosynthetic and growth control pathways affected by HBV. J Med Virol 77: 57-65.
6. Kim KH, Shin HJ, Kim K, Choi HM, Rhee SH, et al. (2007) Hepatitis B virus X protein induces hepatic steatosis via transcriptional activation of SREBP1 and PPARgamma. Gastroenterology 132: 1955-1967.
7. Kim K, Kim KH, Kim HH, Cheong J (2008) Hepatitis B virus X protein induces lipogenic transcription factor SREBP1 and fatty acid synthase through the activation of nuclear receptor LXRalpha. Biochem J 416: 219-230.
8. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
9. Parekh S, Anania FA (2007) Abnormal lipid and glucose metabolism in obesity: implications for nonalcoholic fatty liver disease. Gastroenterology 132: 2191-2207.
10. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116: 1793-1801.
11. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96.
12. Capeau J (2008) Insulin resistance and steatosis in humans. Diabetes Metab 34: 649-657.
13. Yoshimura A, Naka T, Kubo M (2007) SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol 7: 454-465.
14. Krebs DL, Hilton DJ (2000) SOCS: physiological suppressors of cytokine signaling. J Cell Sci 113 (Pt 16): 2813-2819.
15. Klover PJ, Zimmers TA, Koniaris LG, Mooney RA (2003) Chronic exposure to interleukin-6 causes hepatic insulin resistance in mice. Diabetes 52: 2784-2789.
16. Senn JJ, Klover PJ, Nowak IA, Zimmers TA, Koniaris LG, et al. (2003) Suppressor of cytokine signaling-3 (SOCS-3), a potential mediator of interleukin-6-dependent insulin resistance in hepatocytes. J Biol Chem 278: 13740-13746.
17. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, et al. (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 4: 540-545.
18. Barclay JL, Anderson ST, Waters MJ, Curlewis JD (2007) Regulation of suppressor of cytokine signaling 3 (SOC3) by growth hormone in pro-B cells. Mol Endocrinol 21: 2503-2515.
19. Torisu T, Sato N, Yoshiga D, Kobayashi T, Yoshioka T, et al. (2007) The dual function of hepatic SOCS3 in insulin resistance in vivo. Genes Cells 12: 143-154.
20. Rui L, Yuan M, Frantz D, Shoelson S, White MF (2002) SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J Biol Chem 277: 42394-42398.
21. Howard JK, Flier JS (2006) Attenuation of leptin and insulin signaling by SOCS proteins. Trends Endocrinol Metab 17: 365-371.
22. Hui JM, Sud A, Farrell GC, Bandara P, Byth K, et al. (2003) Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression [corrected]. Gastroenterology 125: 1695-1704.
23. Custro N, Carroccio A, Ganci A, Scafidi V, Campagna P, et al. (2001) Glycemic homeostasis in chronic viral hepatitis and liver cirrhosis. Diabetes Metab 27: 476-481.
24. Mohammad Alizadeh AH, Fallahian F, Alavian SM, Ranjbar M, Hedayati M, et al. (2006) Insulin resistance in chronic hepatitis B and C. Indian J Gastroenterol 25: 286-289.
25. Sangiorgio L, Attardo T, Gangemi R, Rubino C, Barone M, et al. (2000) Increased frequency of HCV and HBV infection in type 2 diabetic patients. Diabetes Res Clin Pract 48: 147-151.
26. Masuhara M, Sakamoto H, Matsumoto A, Suzuki R, Yasukawa H, et al. (1997) Cloning and characterization of novel CIS family genes. Biochem Biophys Res Commun 239: 439-446.
27. Yang XP, Albrecht U, Zakowski V, Sobota RM, Haussinger D, et al. (2004) Dual function of interleukin-1beta for the regulation of interleukin-6-induced suppressor of cytokine signaling 3 expression. J Biol Chem 279: 45279-45289.
28. Cha MY, Kim CM, Park YM, Ryu WS (2004) Hepatitis B virus X protein is essential for the activation of Wnt/beta-catenin signaling in hepatoma cells. Hepatology 39: 1683-1693.
29. Guidotti LG, Matzke B, Schaller H, Chisari FV (1995) High-level hepatitis B virus replication in transgenic mice. J Virol 69: 6158-6169.
30. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, et al. (1999) Stat3 as an oncogene. Cell 98: 295-303.
31. Park MJ, Kong HJ, Kim HY, Kim HH, Kim JH, et al. (2007) Transcriptional repression of the gluconeogenic gene PEPCK by the orphan nuclear receptor SHP through inhibitory interaction with C/EBPalpha. Biochem J 402: 567-574.
32. Kong HJ, Park MJ, Hong S, Yu HJ, Lee YC, et al. (2003) Hepatitis B virus X protein regulates transactivation activity and protein stability of the canceramplified transcription coactivator ASC-2. Hepatology 38: 1258-1266.
33. Yu DY, Moon HB, Son JK, Jeong S, Yu SL, et al. (1999) Incidence of hepatocellular carcinoma in transgenic mice expressing the hepatitis B virus Xprotein. J Hepatol 31: 123-132.
34. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, et al. (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336.
35. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, et al. (2002) Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277: 1531-1537.
36. Dandri M, Schirmacher P, Rogler CE (1996) Woodchuck hepatitis virus X protein is present in chronically infected woodchuck liver and woodchuck hepatocellular carcinomas which are permissive for viral replication. J Virol 70: 5246-5254.
37. Auernhammer CJ, Bousquet C, Melmed S (1999) Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc Natl Acad Sci U S A 96: 6964-6969.
38. Krebs DL, Hilton DJ (2001) SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19: 378-387.
39. Wormald S, Hilton DJ (2004) Inhibitors of cytokine signal transduction. J Biol Chem 279: 821-824.
40. Lee YH, Yun Y (1998) HBx protein of hepatitis B virus activates Jak1-STAT signaling. J Biol Chem 273: 25510-25515.
41. Waris G, Huh KW, Siddiqui A (2001) Mitochondrially associated hepatitis B virus X protein constitutively activates transcription factors STAT-3 and NFkappa B via oxidative stress. Mol Cell Biol 21: 7721-7730.
42. Darnell JE, Jr., Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
43. Ihle JN (1995) Cytokine receptor signalling. Nature 377: 591-594.
44. White MF, Kahn CR (1994) The insulin signaling system. J Biol Chem 269: 1-4.
45. O'Brien RM, Granner DK (1996) Regulation of gene expression by insulin. Physiol Rev 76: 1109-1161.
46. Murakami S (2001) Hepatitis B virus X protein: a multifunctional viral regulator. J Gastroenterol 36: 651-660.
47. Fan JG, Chitturi S (2008) Hepatitis B and fatty liver: causal or coincidental? J Gastroenterol Hepatol 23: 679-681.
48. 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.
49. Narazaki M, Fujimoto M, Matsumoto T, Morita Y, Saito H, et al. (1998) Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc Natl Acad Sci U S A 95: 13130-13134.
50. Shimomura I, Matsuda M, Hammer RE, Bashmakov Y, Brown MS, et al. (2000) Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol Cell 6: 77-86.
51. Chen CL, Yang HI, Yang WS, Liu CJ, Chen PJ, et al. (2008) Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan. Gastroenterology 135: 111-121.