Hepatitis B virus pre-S2 mutant induces aerobic glycolysis through mammalian target of rapamycin signal cascade

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Teng, Chiao Fang ^a   Hsieh, Wen Chuan ^a   Wu, Han Chieh ^a   Lin, Yih Jyh ^b   Tsai, Hung Wen ^b   Huang, Wenya ^c   Su, Ih Jen ^a,b  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; PROTEIN EIF4EBP1; RESVERATROL; SILYMARIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YY1; UNCLASSIFIED DRUG; EIF4EBP1 PROTEIN, HUMAN; GLYCOGEN; HEPATITIS B SURFACE ANTIGEN; MUTANT PROTEIN; PHOSPHOPROTEIN; PRESURFACE PROTEIN 2, HEPATITIS B SURFACE ANTIGEN; PROTEIN PRECURSOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE;

AEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; GENE EXPRESSION PROFILING; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HEPATITIS B VIRUS; HUMAN; HUMAN TISSUE; IN VITRO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VIRUS MUTANT; ANIMAL; CARCINOMA, HEPATOCELLULAR; CELL LINE; GENETICS; HEPATITIS B; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; VIROLOGY;

EUKARYOTA; HEPATITIS B VIRUS; MAMMALIA; MUS MUSCULUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE; GLUCOSE TRANSPORTER TYPE 1; GLYCOGEN; GLYCOLYSIS; HEPATITIS B; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MICE; MICE, TRANSGENIC; MUTANT PROTEINS; PHOSPHOPROTEINS; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; YY1 TRANSCRIPTION FACTOR;

EID: 84929309929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122373     Document Type: Article

References (37)

1. Beasley RP, Hwang LY, Lin CC, Chien CS. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet. 1981; 2: 1129-1133. PMID: 6118576
2. Sitia G, Aiolfi R, Di Lucia P, Mainetti M, Fiocchi A, Mingozzi F, et al. Antiplatelet therapy prevents hepatocellular carcinoma and improves survival in a mouse model of chronic hepatitis B. Proc Natl Acad Sci U S A. 2012; 109: E2165-2172. doi: 10.1073/pnas.1209182109 PMID: 22753481
3. Su IJ, Hsieh WC, Tsai HW, Wu HC. Chemoprevention and novel therapy for hepatocellular carcinoma associated with chronic hepatitis B virus infection. Hepatobiliary Surg Nutr. 2013; 2: 37-39. doi: 10.3978/j.issn.2304-3881.2012.10.08 PMID: 24570914
4. Wang HC, Huang W, Lai MD, Su IJ. Hepatitis B virus pre-S mutants, endoplasmic reticulum stress and hepatocarcinogenesis. Cancer Sci. 2006; 97: 683-688. PMID: 16863502
5. Wang HC, Chang WT, Chang WW, Wu HC, Huang W, Lei HY, et al. Hepatitis B virus pre-S2 mutant upregulates cyclin A expression and induces nodular proliferation of hepatocytes. Hepatology. 2005; 41: 761-770. PMID: 15726643
6. Chen CH, Hung CH, Lee CM, Hu TH, Wang JH, Wang JC, et al. Pre-S deletion and complex mutations of hepatitis B virus related to advanced liver disease in HBeAg-negative patients. Gastroenterology. 2007; 133: 1466-1474. PMID: 17915220
7. Tsai HW, Lin YJ, Lin PW, Wu HC, Hsu KH, Yen CJ, et al. A clustered ground-glass hepatocyte pattern represents a new prognostic marker for the recurrence of hepatocellular carcinoma after surgery. Cancer. 2011; 117: 2951-2960. doi: 10.1002/cncr.25837 PMID: 21692054
8. Wu HC, Tsai HW, Teng CF, Hsieh WC, Lin YJ, Wang LH, et al. Ground-glass hepatocytes co-expressing hepatitis B virus X protein and surface antigens exhibit enhanced oncogenic effects and tumorigenesis. Hum Pathol. 2014; 45:1294-1301. doi: 10.1016/j.humpath.2013.10.039 PMID: 24767856
9. Su IJ, Wang HC, Wu HC, Huang WY. Ground glass hepatocytes contain pre-S mutants and represent preneoplastic lesions in chronic hepatitis B virus infection. J Gastroenterol Hepatol. 2008; 23: 1169-1174. doi: 10.1111/j.1440-1746.2008.05348.x PMID: 18505413
10. Pollicino T, Cacciola I, Saffioti F, Raimondo G. Hepatitis B virus PreS/S gene variants: Pathobiology and clinical implications. J Hepatol. 2014; 61: 408-417. doi: 10.1016/j.jhep.2014.04.041 PMID: 24801416
11. Cantor JR, Sabatini DM. Cancer cell metabolism: one hallmark, many faces. Cancer Discov. 2012; 2: 881-898. doi: 10.1158/2159-8290.CD-12-0345 PMID: 23009760
12. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008; 134: 703-707. doi: 10.1016/j.cell.2008.08.021 PMID: 18775299
13. Bannasch P. Glycogenotic hepatocellular carcinoma with glycogen-ground-glass hepatocytes: a heuristically highly relevant phenotype. World J Gastroenterol. 2012; 18: 6701-6708. doi: 10.3748/wjg.v18.i46.6701 PMID: 23239906
14. Beyoglu D, Imbeaud S, Maurhofer O, Bioulac-Sage P, Zucman-Rossi J, Dufour JF, et al. Tissue metabolomics of hepatocellular carcinoma: Tumor energy metabolism and the role of transcriptomic classification. Hepatology. 2013; 58: 229-238. doi: 10.1002/hep.26350 PMID: 23463346
15. Huang Q, Tan Y, Yin P, Ye G, Gao P, Lu X, et al. Metabolic characterization of hepatocellular carcinoma using nontargeted tissue metabolomics. Cancer Res. 2013; 73: 4992-5002. doi: 10.1158/0008-5472.CAN-13-0308 PMID: 23824744
16. Toshkov I, Chisari FV, Bannasch P. Hepatic preneoplasia in hepatitis B virus transgenic mice. Hepatology. 1994; 20: 1162-1172. PMID: 7927248
17. Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci. 2009; 122: 3589-3594. doi: 10.1242/jcs.051011 PMID: 19812304
18. Cornu M, Albert V, Hall MN. mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev. 2013; 23: 53-62. doi: 10.1016/j.gde.2012.12.005 PMID: 23317514
19. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell. 2010; 39: 171-183. doi: 10.1016/j.molcel.2010.06.022 PMID: 20670887
20. Yang JC, Teng CF, Wu HC, Tsai HW, Chuang HC, Tsai TF, et al. Enhanced expression of vascular endothelial growth factor-A in ground glass hepatocytes and its implication in hepatitis B virus hepatocarcinogenesis. Hepatology. 2009; 49: 1962-1971. doi: 10.1002/hep.22889 PMID: 19475690
21. Teng CF, Wu HC, Tsai HW, Shiah HS, Huang W, Su IJ. Novel feedback inhibition of surface antigen synthesis by mammalian target of rapamycin (mTOR) signal and its implication for hepatitis B virus tumorigenesis and therapy. Hepatology. 2011; 54: 1199-1207. doi: 10.1002/hep.24529 PMID: 21735472
22. Zhang Q, Stovall DB, Inoue K, Sui G. The oncogenic role of Yin Yang 1. Crit Rev Oncog. 2011; 16: 163-197. PMID: 22248053
23. Wu BK, Li CC, Chen HJ, Chang JL, Jeng KS, Chou CK, et al. Blocking of G1/S transition and cell death in the regenerating liver of Hepatitis B virus X protein transgenic mice. Biochem Biophys Res Commun. 2006; 340: 916-928. PMID: 16403455
24. Miller DM, Thomas SD, Islam A, Muench D, Sedoris K. c-Myc and Cancer Metabolism. Clin Cancer Res. 2012; 18: 5546-5553. doi: 10.1158/1078-0432.CCR-12-0977 PMID: 23071356
25. Amann T, Hellerbrand C. GLUT1 as a therapeutic target in hepatocellular carcinoma. Expert Opin Ther Targets. 2009; 13: 1411-1427. doi: 10.1517/14728220903307509 PMID: 19874261
26. Joe AK, Liu H, Suzui M, Vural ME, Xiao D, Weinstein IB. Resveratrol induces growth inhibition, S- phase arrest, apoptosis, and changes in biomarker expression in several human cancer cell lines. Clin Cancer Res. 2002; 8: 893-903. PMID: 11895924
27. Agarwal R, Agarwal C, Ichikawa H, Singh RP, Aggarwal BB. Anticancer potential of silymarin: from bench to bed side. Anticancer Res. 2006; 26: 4457-4498. PMID: 17201169
28. Hsieh WC, Yang CW, Huang YS, Chao TW, Tsai TF, Su IJ. Chemoprevention of HBV-related hepatocellular carcinoma by the combined product of resveratrol and silymarin in transgenic mice. Functional Foods in Health and Disease. 2013; 3: 341-352.
29. Zha X, Sun Q, Zhang H. mTOR upregulation of glycolytic enzymes promotes tumor development. Cell Cycle. 2011; 10: 1015-1016. PMID: 21393998
30. Amann T, Maegdefrau U, Hartmann A, Agaimy A, Marienhagen J, Weiss TS, et al. GLUT1 expression is increased in hepatocellular carcinoma and promotes tumorigenesis. Am J Pathol. 2009; 174: 1544-1552. doi: 10.2353/ajpath.2009.080596 PMID: 19286567
31. Sankar N, Baluchamy S, Kadeppagari RK, Singhal G, Weitzman S, Thimmapaya B. p300 provides a corepressor function by cooperating with YY1 And HDAC3 to repress c-Myc. Oncogene. 2008; 27: 5717-5728. doi: 10.1038/onc.2008.181 PMID: 18542060
32. Hu HM, Kanda K, Zhang L, Boxer LM. Activation of the c-myc p1 promoter in Burkitt's lymphoma by the hs3 immunoglobulin heavy-chain gene enhancer. Leukemia. 2007; 21: 747-753. PMID: 17287852
33. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, et al. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature. 2012; 485: 55-61. doi: 10.1038/nature10912 PMID: 22367541
34. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature. 2012; 485: 109-113. doi: 10.1038/nature11083 PMID: 22552098
35. Bishayee A, Politis T, Darvesh AS. Resveratrol in the chemoprevention and treatment of hepatocellular carcinoma. Cancer Treat Rev. 2010; 36: 43-53. doi: 10.1016/j.ctrv.2009.10.002 PMID: 19910122
36. Feher J, Lengyel G. Silymarin in the prevention and treatment of liver diseases and primary liver cancer. Curr Pharm Biotechnol. 2012; 13: 210-217. PMID: 21466434
37. Jiang H, Shang X, Wu H, Gautam SC, Al-Holou S, Li C, et al. Resveratrol downregulates PI3K/Akt/ mTOR signaling pathways in human U251 glioma cells. J Exp Ther Oncol. 2009; 8: 25-33. PMID: 19827268