Hepatitis B virus X (HBx) induces tumorigenicity of hepatic progenitor cells in 3,5-diethoxycarbonyl-1,4-dihydrocollidine-treated HBx transgenic mice

Hepatology

Volumn 55, Issue 1, 2012, Pages 108-120

  Wang, Chao ^a   Yang, Wen ^a   Yan, He Xin ^a   Luo, Tao ^a   Zhang, Jian ^a   Tang, Liang ^a   Wu, Fu Quan ^a   Zhang, Hui Lu ^a   Yu, Le Xing ^a   Zheng, Long Yi ^a   Li, Yu Qiong ^a   Dong, Wei ^a   He, Ya Qin ^a   Liu, Qiong ^a   Zou, Shan Shan ^a   Lin, Yan ^a   Hu, Liang ^a   Li, Zhong ^a   Wu, Meng Chao ^a   Wang, Hong Yang ^a,b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SHANGHAI CANCER INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,4,6 TRIMETHYL 3,5 PYRIDINEDICARBOXYLIC ACID DIETHYL ESTER; BETA CATENIN; HEPATITIS B VIRUS X PROTEIN; INTERLEUKIN 6; STAT3 PROTEIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT CARCINOMA; CANCER INCIDENCE; CARCINOGENICITY; CELL COUNT; CLINICAL FEATURE; CONTROLLED STUDY; FLOW CYTOMETRY; HEPATITIS B VIRUS; HUMAN; HUMAN TISSUE; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER INJURY; LIVER TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TRANSGENIC MOUSE; TUMOR GROWTH;

ANIMALS; BILE DUCT NEOPLASMS; BILE DUCTS, INTRAHEPATIC; CARCINOMA, HEPATOCELLULAR; CELL TRANSFORMATION, NEOPLASTIC; CHOLANGIOCARCINOMA; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MIDDLE AGED; PYRIDINES; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATORS;

EID: 84155180684     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24675     Document Type: Article

References (37)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. GLOBOCAN 2008 v1.2, Cancer Incidence and Mortality Worldwide. IARC CancerBase No. 10.
2. Brechot C, Pourcel C, Louise A, Rain B, Tiollais P. Presence of integrated hepatitis B virus DNA sequences in cellular DNA of human hepatocellular carcinoma. Nature 1980; 286: 533-535.
3. Benhenda S, Cougot D, Buendia MA, Neuveut C. Hepatitis B virus X protein molecular functions and its role in virus life cycle and pathogenesis. Adv Cancer Res 2009; 103: 75-109.
4. Sung WK, Lu Y, Lee CW, Zhang D, Ronaghi M, Lee CG. Deregulated direct targets of the hepatitis B virus (HBV) protein, HBx, identified through chromatin immunoprecipitation and expression microarray profiling. J Biol Chem 2009; 284: 21941-21954.
5. Wang Y, Cui F, Lv Y, Li C, Xu X, Deng C, et al. HBsAg and HBx knocked into the p21 locus causes hepatocellular carcinoma in mice. HEPATOLOGY 2004; 39: 318-324.
6. Germain L, Noel M, Gourdeau H, Marceau N. Promotion of growth and differentiation of rat ductular oval cells in primary culture. Cancer Res 1988; 48: 368-378.
7. Paku S, Nagy P, Kopper L, Thorgeirsson SS. 2-Acetylaminofluorene dose-dependent differentiation of rat oval cells into hepatocytes: confocal and electron microscopic studies. HEPATOLOGY 2004; 39: 1353-1361.
8. Wang X, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M. The origin and liver repopulating capacity of murine oval cells. Proc Natl Acad Sci U S A 2003; 100(Suppl 1): 11881-11888.
9. Petersen BE, Goff JP, Greenberger JS, Michalopoulos GK. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. HEPATOLOGY 1998; 27: 433-445.
10. Hu M, Kurobe M, Jeong YJ, Fuerer C, Ghole S, Nusse R, et al. Wnt/beta-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 2007; 133: 1579-1591.
11. Apte U, Thompson MD, Cui S, Liu B, Cieply B, Monga SP. Wnt/beta-catenin signaling mediates oval cell response in rodents. HEPATOLOGY 2008; 47: 288-295.
12. Yang W, Yan HX, Chen L, Liu Q, He YQ, Yu LX, et al. Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells. Cancer Res 2008; 68: 4287-4295.
13. Tang Y, Kitisin K, Jogunoori W, Li C, Deng CX, Mueller SC, et al. Progenitor/stem cells give rise to liver cancer due to aberrant TGF-beta and IL-6 signaling. Proc Natl Acad Sci U S A 2008; 105: 2445-2450.
14. Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, Onodera M, et al. Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology 2007; 133: 937-950.
15. Lee KP, Lee JH, Kim TS, Kim TH, Park HD, Byun JS, et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci U S A 2010; 107: 8248-8253.
16. Suzuki A, Sekiya S, Onishi M, Oshima N, Kiyonari H, Nakauchi H, et al. Flow cytometric isolation and clonal identification of self-renewing bipotent hepatic progenitor cells in adult mouse liver. HEPATOLOGY 2008; 48: 1964-1978.
17. Lowes KN, Brennan BA, Yeoh GC, Olynyk JK. Oval cell numbers in human chronic liver diseases are directly related to disease severity. Am J Pathol 1999; 154: 537-541.
18. Okabe M, Tsukahara Y, Tanaka M, Suzuki K, Saito S, Kamiya Y, et al. Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver. Development 2009; 136: 1951-1960.
19. Beer S, Komatsubara K, Bellovin DI, Kurobe M, Sylvester K, Felsher DW. Hepatotoxin-induced changes in the adult murine liver promote MYC-induced tumorigenesis. PLoS One 2008; 3: e2493.
20. Matthews VB, Klinken E, Yeoh GC. Direct effects of interleukin-6 on liver progenitor oval cells in culture. Wound Repair Regen 2004; 12: 650-656.
21. Xiang WQ, Feng WF, Ke W, Sun Z, Chen Z, Liu W. Hepatitis B virus X protein stimulates IL-6 expression in hepatocytes via a MyD88-dependent pathway. J Hepatol 2011; 54: 26-33.
22. Ding Q, Xia W, Liu JC, Yang JY, Lee DF, Xia J, et al. Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol Cell 2005; 19: 159-170.
23. Yamashita T, Ji J, Budhu A, Forgues M, Yang W, Wang HY, et al. EpCAM-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology 2009; 136: 1012-1024.
24. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006; 355: 1253-1261.
25. Sell S, Leffert HL. Liver cancer stem cells. J Clin Oncol 2008; 26: 2800-2805.
26. Galicia VA, He L, Dang H, Kanel G, Vendryes C, French BA, et al. Expansion of hepatic tumor progenitor cells in Pten-null mice requires liver injury and is reversed by loss of AKT2. Gastroenterology 2010; 139: 2170-2182.
27. Ziol M, Nault JC, Aout M, Barget N, Tepper M, Martin A, et al. Intermediate hepatobiliary cells predict an increased risk of hepatocarcinogenesis in patients with hepatitis C virus-related cirrhosis. Gastroenterology 2010; 139: 335-343 e332.
28. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 2006; 12: 410-416.
29. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995; 82: 675-684.
30. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007; 317: 121-124.
31. Abiru S, Migita K, Maeda Y, Daikoku M, Ito M, Ohata K, et al. Serum cytokine and soluble cytokine receptor levels in patients with non-alcoholic steatohepatitis. Liver Int 2006; 26: 39-45.
32. Wong VW, Yu J, Cheng AS, Wong GL, Chan HY, Chu ES, et al. High serum interleukin-6 level predicts future hepatocellular carcinoma development in patients with chronic hepatitis B. Int J Cancer 2009; 124: 2766-2770.
33. Thompson MD, Monga SP. WNT/beta-catenin signaling in liver health and disease. HEPATOLOGY 2007; 45: 1298-1305.
34. Cha MY, Kim CM, Park YM, Ryu WS. Hepatitis B virus X protein is essential for the activation of Wnt/beta-catenin signaling in hepatoma cells. HEPATOLOGY 2004; 39: 1683-1693.
35. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007; 120: 1444-1450.
36. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007; 132: 2542-2556.
37. Arzumanyan A, Friedman T, Ng IO, Clayton M, Lian Z, Feitelson MA. Does the hepatitis B antigen HBx promote the appearance of liver cancer stem cells? Cancer Res 2011; 71: 3701-3708.