HBx regulates fatty acid oxidation to promote hepatocellular carcinoma survival during metabolic stress

Oncotarget

Volumn 7, Issue 6, 2016, Pages 6711-6726

  Wang, Ming Da ^a,b   Wu, Han ^a   Huang, Shuai ^a   Zhang, Hui Lu ^a   Qin, Chen Jie ^a,b   Zhao, Ling Hao ^a   Fu, Gong Bo ^a,b   Zhou, Xu ^a,b   Wang, Xian Ming ^a,b   Tang, Liang ^a   Wen, Wen ^a,b   Yang, Wen ^a,b   Tang, Shan Hua ^a,b   Cao, Dan ^a,b   Guo, Lin Na ^a,b   Zeng, Min ^a,b   Wu, Meng Chao ^a   Yan, He Xin ^a,b   Wang, Hong Yang ^a,b,c  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b National Center for Liver Cancer   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Cell survival; Energy homeostasis; Fatty acid oxidation; Hepatitis B virus X protein; Metabolic stress

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE INHIBITOR; CARNITINE PALMITOYLTRANSFERASE I; ETOMOXIR; HEPATITIS B VIRUS X PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA; STO 609; UNCLASSIFIED DRUG; FATTY ACID; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; FATTY ACID OXIDATION; GLYCOLYSIS; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; UPREGULATION; ANIMAL; BIOSYNTHESIS; DEFICIENCY; GENETICS; HEP-G2 CELL LINE; LIPID METABOLISM; LIVER TUMOR; METABOLISM; NUDE MOUSE; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL SURVIVAL; FATTY ACIDS; GLUCOSE; GLYCOLYSIS; HEP G2 CELLS; HETEROGRAFTS; HUMANS; LIPID METABOLISM; LIVER NEOPLASMS; MALE; MICE; MICE, NUDE; NADP; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; UP-REGULATION;

EID: 84981212368     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6817     Document Type: Article

References (53)

1. Marrero JA. Hepatocellular carcinoma. Current opinion in gastroenterology. 2006; 22:248-253.
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. Advances in cancer research. 2009; 103:75-109.
4. Feitelson MA, Duan LX. Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. The American journal of pathology. 1997; 150:1141-1157.
5. Henkler FF, Koshy R. Hepatitis B virus transcriptional activators: mechanisms and possible role in oncogenesis. Journal of viral hepatitis. 1996; 3:109-121.
6. Huang J, Kwong J, Sun EC, Liang TJ. Proteasome complex as a potential cellular target of hepatitis B virus X protein. Journal of virology. 1996; 70:5582-5591.
7. Zheng DL, Zhang L, Cheng N, Xu X, Deng Q, Teng XM, Wang KS, Zhang X, Huang J, Han ZG. Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. Journal of hepatology. 2009; 50:377-387.
8. Dang CV. Links between metabolism and cancer. Genes & development. 2012; 26:877-890.
9. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 2010; 330:1340-1344.
10. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
11. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009; 324:1029-1033.
12. Warburg O. On the origin of cancer cells. Science. 1956; 123:309-314.
13. Currie E, Schulze A, Zechner R, Walther TC, Farese RV, Jr. Cellular fatty acid metabolism and cancer. Cell metabolism. 2013; 18:153-161.
14. Schulze A, Harris AL. How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature. 2012; 491:364-373.
15. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008; 134:703-707.
16. Hirayama A, Kami K, Sugimoto M, Sugawara M, Toki N, Onozuka H, Kinoshita T, Saito N, Ochiai A, Tomita M, Esumi H, Soga T. Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry. Cancer research. 2009; 69:4918-4925.
17. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, Foretz M, Viollet B. 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Molecular and cellular biology. 2006; 26:5336-5347.
18. Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nature reviews Cancer. 2011; 11:85-95.
19. Jeon SM, Chandel NS, Hay N. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature. 2012; 485:661-665.
20. Samudio I, Harmancey R, Fiegl M, Kantarjian H, Konopleva M, Korchin B, Kaluarachchi K, Bornmann W, Duvvuri S, Taegtmeyer H, Andreeff M. Pharmacologic inhibition of fatty acid oxidation sensitizes human leukemia cells to apoptosis induction. The Journal of clinical investigation. 2010; 120:142-156.
21. Zaugg K, Yao Y, Reilly PT, Kannan K, Kiarash R, Mason J, Huang P, Sawyer SK, Fuerth B, Faubert B, Kalliomaki T, Elia A, Luo X, et al. Carnitine palmitoyltransferase 1C promotes cell survival and tumor growth under conditions of metabolic stress. Genes & development. 2011; 25:1041-1051.
22. Carracedo A, Weiss D, Leliaert AK, Bhasin M, de Boer VC, Laurent G, Adams AC, Sundvall M, Song SJ, Ito K, Finley LS, Egia A, Libermann T, et al. A metabolic prosurvival role for PML in breast cancer. The Journal of clinical investigation. 2012; 122:3088-3100.
23. Cabodevilla AG, Sanchez-Caballero L, Nintou E, Boiadjieva VG, Picatoste F, Gubern A, Claro E. Cell survival during complete nutrient deprivation depends on lipid droplet-fueled beta-oxidation of fatty acids. The Journal of biological chemistry. 2013; 288:27777-27788.
24. Cui M, Xiao Z, Sun B, Wang Y, Zheng M, Ye L, Zhang X. Involvement of cholesterol in hepatitis B virus X protein-induced abnormal lipid metabolism of hepatoma cells via up-regulating miR-205-targeted ACSL4. Biochemical and biophysical research communications. 2014; 445:651-655.
25. You X, Liu F, Zhang T, Li Y, Ye L, Zhang X. Hepatitis B virus X protein upregulates oncogene Rab18 to result in the dysregulation of lipogenesis and proliferation of hepatoma cells. Carcinogenesis. 2013; 34:1644-1652.
26. Kim KH, Shin HJ, Kim K, Choi HM, Rhee SH, Moon HB, Kim HH, Yang US, Yu DY, Cheong J. Hepatitis B virus X protein induces hepatic steatosis via transcriptional activation of SREBP1 and PPARgamma. Gastroenterology. 2007; 132:1955-1967.
27. Kim JY, Song EH, Lee HJ, Oh YK, Choi KH, Yu DY, Park SI, Seong JK, Kim WH. HBx-induced hepatic steatosis and apoptosis are regulated by TNFR1- and NF-kappaB-dependent pathways. Journal of molecular biology. 2010; 397:917-931.
28. Bungard D, Fuerth BJ, Zeng PY, Faubert B, Maas NL, Viollet B, Carling D, Thompson CB, Jones RG, Berger SL. Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science. 2010; 329:1201-1205.
29. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. The Journal of biological chemistry. 2005; 280: 29060-29066.
30. Bouchard MJ, Wang LH, Schneider RJ. Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science. 2001; 294:2376-2378.
31. Clapham DE. Calcium signaling. Cell. 1995; 80:259-268.
32. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R. STO-609, a specific inhibitor of the Ca(2+)/calmodulin-dependent protein kinase kinase. The Journal of biological chemistry. 2002; 277:15813-15818.
33. Liu L, Zhang J, Li M, Zhang X, Li Z, Wang L, Wu J, Luo C. Inhibition of HepG2 cell proliferation by ursolic acid and polysaccharides via the downregulation of cyclooxygenase-2. Molecular medicine reports. 2014; 9:2505-2511.
34. Li JL, Wang QY, Luan HY, Kang ZC, Wang CB. Effects of L-carnitine against oxidative stress in human hepatocytes: involvement of peroxisome proliferator-activated receptor alpha. Journal of biomedical science. 2012; 19:32.
35. Na TY, Shin YK, Roh KJ, Kang SA, Hong I, Oh SJ, Seong JK, Park CK, Choi YL, Lee MO. Liver X receptor mediates hepatitis B virus X protein-induced lipogenesis in hepatitis B virus-associated hepatocellular carcinoma. Hepatology. 2009; 49:1122-1131.
36. Boren J, Brindle KM. Apoptosis-induced mitochondrial dysfunction causes cytoplasmic lipid droplet formation. Cell death and differentiation. 2012; 19:1561-1570.
37. Du L, Hickey RW, Bayir H, Watkins SC, Tyurin VA, Guo F, Kochanek PM, Jenkins LW, Ren J, Gibson G, Chu CT, Kagan VE, Clark RS. Starving neurons show sex difference in autophagy. The Journal of biological chemistry. 2009; 284:2383-2396.
38. Lei P, Baysa A, Nebb HI, Valen G, Skomedal T, Osnes JB, Yang Z, Haugen F. Activation of Liver X receptors in the heart leads to accumulation of intracellular lipids and attenuation of ischemia-reperfusion injury. Basic research in cardiology. 2013; 108:323.
39. Zwaans BM, Lombard DB. Interplay between sirtuins, MYC and hypoxia-inducible factor in cancer-associated metabolic reprogramming. Disease models & mechanisms. 2014; 7:1023-1032.
40. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, Rajagopalan H, Schmidt K, Willson JK, Markowitz S, Zhou S, Diaz LA, Jr., Velculescu VE, Lengauer C, Kinzler KW, Vogelstein B, Papadopoulos N. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science. 2009; 325:1555-1559.
41. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, Gottlieb E, Vousden KH. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell. 2006; 126:107-120.
42. Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nature reviews Cancer. 2009; 9:563-575.
43. Hong SP, Momcilovic M, Carlson M. Function of mammalian LKB1 and Ca2+/calmodulin-dependent protein kinase kinase alpha as Snf1-activating kinases in yeast. The Journal of biological chemistry. 2005; 280:21804-21809.
44. Oh JC, Jeong DL, Kim IK, Oh SH. Activation of calcium signaling by hepatitis B virus-X protein in liver cells. Experimental & molecular medicine. 2003; 35:301-309.
45. Faubert B, Boily G, Izreig S, Griss T, Samborska B, Dong Z, Dupuy F, Chambers C, Fuerth BJ, Viollet B, Mamer OA, Avizonis D, DeBerardinis RJ, Siegel PM, Jones RG. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell metabolism. 2013; 17:113-124.
46. Buzzai M, Jones RG, Amaravadi RK, Lum JJ, DeBerardinis RJ, Zhao F, Viollet B, Thompson CB. Systemic treatment with the antidiabetic drug metformin selectively impairs p53-deficient tumor cell growth. Cancer research. 2007; 67:6745-6752.
47. Huang X, Wullschleger S, Shpiro N, McGuire VA, Sakamoto K, Woods YL, McBurnie W, Fleming S, Alessi DR. Important role of the LKB1-AMPK pathway in suppressing tumorigenesis in PTEN-deficient mice. The Biochemical journal. 2008; 412:211-221.
48. Zheng L, Yang W, Wu F, Wang C, Yu L, Tang L, Qiu B, Li Y, Guo L, Wu M, Feng G, Zou D, Wang H. Prognostic significance of AMPK activation and therapeutic effects of metformin in hepatocellular carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 2013; 19:5372-5380.
49. Marra M, Sordelli IM, Lombardi A, Lamberti M, Tarantino L, Giudice A, Stiuso P, Abbruzzese A, Sperlongano R, Accardo M, Agresti M, Caraglia M, Sperlongano P. Molecular targets and oxidative stress biomarkers in hepatocellular carcinoma: an overview. J Transl Med. 2011; 9:171.
50. Qian YW, Chen Y, Yang W, Fu J, Cao J, Ren YB, Zhu JJ, Su B, Luo T, Zhao XF, Dai RY, Li JJ, Sun W, Wu MC, Feng GS, Wang HY. p28(GANK) prevents degradation of Oct4 and promotes expansion of tumor-initiating cells in hepatocarcinogenesis. Gastroenterology. 2012; 142:1547-1558 e1514.
51. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CAt, Ramalho-Santos J, Van Houten B, Schatten G. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PloS one. 2011; 6:e20914.
52. Zhang JW, Zhang SS, Song JR, Sun K, Zong C, Zhao QD, Liu WT, Li R, Wu MC, Wei LX. Autophagy inhibition switches low-dose camptothecin-induced premature senescence to apoptosis in human colorectal cancer cells. Biochemical pharmacology. 2014; 90:265-275.
53. Wang RY, Chen L, Chen HY, Hu L, Li L, Sun HY, Jiang F, Zhao J, Liu GM, Tang J, Chen CY, Yang YC, Chang YX, et al. MUC15 inhibits dimerization of EGFR and PI3K-AKT signaling and is associated with aggressive hepatocellular carcinomas in patients. Gastroenterology. 2013; 145:1436-1448 e1431-1412.