A specific cholesterol metabolic pathway is established in a subset of HCCs for tumor growth

Journal of Molecular Cell Biology

Volumn 5, Issue 6, 2013, Pages 404-415

  Lu, Ming ^a   Hu, Xi Han ^a   Li, Qin ^a   Xiong, Ying ^a   Hu, Guang Jing ^a   Xu, Jia Jia ^a   Zhao, Xiao Nan ^a   Wei, Xi Xiao ^a   Chang, Catherine C Y ^b   Liu, Yin Kun ^c   Nan, Fa Jun ^d   Li, Jia ^d   Chang, Ta Yuan ^b   Song, Bao Liang ^a   Li, Bo Liang ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c FUDAN UNIVERSITY   (China)

^d SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

ACAT2; CpG methylation; HCC; Inhibition of tumor growth; Oxysterol secretion

Indexed keywords

APOLIPOPROTEIN B100; CHOLESTEROL ACYLTRANSFERASE; OXYSTEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER PATIENT; CANCER TISSUE; CHOLESTEROL ESTERIFICATION; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; CYTOTOXICITY; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PROMOTER REGION; SECRETION (PROCESS); XENOGRAFT;

ACAT2; CPG METHYLATION; HCC; INHIBITION OF TUMOR GROWTH; OXYSTEROL SECRETION;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHOLESTEROL; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE, NUDE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84890403036     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjt039     Document Type: Article

References (51)

1. Bemlih, S., Poirier, M.D., and El Andaloussi, A. (2010). Acyl-coenzyme A: cholesterol acyltransferase inhibitor Avasimibe affect survival and proliferation of glioma tumor cell lines. Cancer Biol. Ther. 9, 1025-1032.
2. Bjorkhem, I., Diczfalusy, U., and Lutjohann, D. (1999). Removal of cholesterol from extrahepatic sources by oxidative mechanisms. Curr. Opin. Lipidol. 10, 161-165.
3. Bjorkhem, I., Meaney, S., and Diczfalusy, U. (2002). Oxysterols in human circulation: which role do they have? Curr. Opin. Lipidol. 13, 247-253.
4. Bocan, T.M., Krause, B.R., Rosebury, W.S., et al. (2000). The ACAT inhibitor avasimibe reduces macrophages and matrix metalloproteinase expression in atherosclerotic lesions of hypercholesterolemic rabbits. Arterioscler. Thromb. Vasc. Biol. 20, 70-79.
5. Brown, A.J., and Jessup, W. (2009). Oxysterols: sources, cellular storage and metabolism, and new insights into their roles in cholesterol homeostasis. Mol. Aspects Med. 30, 111-122.
6. Buhman, K.K., Accad, M., Novak, S., et al. (2000). Resistance to diet-induced hypercholesterolemia and gallstone formation in ACAT2-deficient mice. Nat. Med. 6, 1341-1347.
7. Burkard, I., von Eckardstein, A., Waeber, G., et al. (2007). Lipoprotein distribution and biological variation of 24S-and 27-hydroxycholesterol in healthy volunteers. Atherosclerosis 194, 71-78.
8. Cases, S., Novak, S., Zheng, Y.W., et al. (1998). ACAT-2, a second mammalian acyl-CoA:cholesterol acyltransferase. Its cloning, expression, and characterization. J. Biol. Chem. 273, 26755-26764.
9. Chang, C.C., Sakashita, N., Ornvold, K., et al. (2000). Immunological quantitation and localization of ACAT-1 and ACAT-2 in human liver and small intestine. J. Biol. Chem. 275, 28083-28092.
10. Chang, T.Y., Li, B.L., Chang, C.C., et al. (2009). Acyl-coenzyme A:cholesterol acyltransferases. Am. J. Physiol. Endocrinol. Metab. 297, E1-E9.
11. Dashti, N. (1992). The effect of low density lipoproteins, cholesterol, and 25-hydroxycholesterol on apolipoprotein B gene expression in HepG2 cells. J. Biol. Chem. 267, 7160-7169.
12. De Berardinis, R.J., Lum, J.J., Hatzivassiliou, G., et al. (2008). The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7, 11-20.
13. de Lope, C.R., Tremosini, S., Forner, A., et al. (2012). Management of HCC. J. Hepatol. 56(Suppl 1), S75-S87.
14. Dietschy, J.M., Turley, S.D., and Spady, D.K. (1993). Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J. Lipid Res. 34, 1637-1659.
15. El-Serag, H.B. (2012). Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142, 1264-1273.e1.
16. Forner, A., Llovet, J.M., and Bruix, J. (2012). Hepatocellular carcinoma. Lancet 379, 1245-1255.
17. Gill, S., Chow, R., and Brown, A.J. (2008). Sterol regulators of cholesterol homeostasis and beyond: the oxysterol hypothesis revisited and revised. Prog. Lipid Res. 47, 391-404.
18. Goldstein, J.L., Basu, S.K., and Brown, M.S. (1983). Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98, 241-260.
19. Grefhorst, A., Elzinga, B.M., Voshol, P.J., et al. (2002). Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 277, 34182-34190.
20. Higashi, Y., Itabe, H., Fukase, H., et al. (2002). Distribution of microsomal triglyceride transfer protein within sub-endoplasmic reticulum regions in human hepatoma cells. Biochim. Biophys. Acta 1581, 127-136.
21. Hutter-Paier, B., Huttunen, H.J., Puglielli, L., et al. (2004). The ACAT inhibitor CP-113,818 markedly reduces amyloid pathology in a mouse model of Alzheimer's disease. Neuron 44, 227-238.
22. Ikenoya, M., Yoshinaka, Y., Kobayashi, H., et al. (2007). Aselective ACAT-1 inhibitor, K-604, suppresses fatty streak lesions in fat-fed hamsters without affecting plasma cholesterol levels. Atherosclerosis 191, 290-297.
23. Jones, P.A., and Takai, D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293, 1068-1070.
24. Kusunoki, J., Hansoty, D.K., Aragane, K., et al. (2001). Acyl-CoA:cholesterol acyltransferase inhibition reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 103, 2604-2609.
25. Lachner, M., O'Sullivan, R.J., and Jenuwein, T. (2003). An epigenetic roadmap for histone lysine methylation. J. Cell Sci. 116, 2117-2124.
26. Lee, R.G., Shah, R., Sawyer, J.K., et al. (2005). ACAT2 contributes cholesteryl esters to newly secreted VLDL, whereas LCAT adds cholesteryl ester to LDL in mice. J. Lipid Res. 46, 1205-1212.
27. Lin, C.Y., and Morel, D.W. (1996). Esterification of oxysterols in human serum: effects on distribution and cellular uptake. J. Lipid Res. 37, 168-178.
28. Liu, J., Chang, C.C., Westover, E.J., et al. (2005). Investigating the allosterism of acyl-CoA:cholesterol acyltransferase (ACAT) by using various sterols: in vitro and intact cell studies. Biochem. J. 391, 389-397.
29. Llovet, J.M., Ricci, S., Mazzaferro, V., et al. (2008). Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med. 359, 378-390.
30. Meex, S.J., Andreo, U., and Sparks, J.D., et al. (2011). Huh-7 orHepG2 cells: which is the better model for studyinghumanapolipoprotein-B100 assemblyand secretion? J. Lipid Res. 52, 152-158.
31. Monte, M.J., Fernandez-Tagarro, M., Macias, R.I., et al. (2005). Changes in the expression of genes related to bile acid synthesis and transport by the rat liver during hepatocarcinogenesis. Clin. Sci. (Lond) 109, 199-207.
32. Ohshiro, T., Rudel, L.L., Omura, S., et al. (2007). Selectivity of microbial acyl-CoA: cholesterol acyltransferase inhibitors toward isozymes. J. Antibiot. (Tokyo) 60, 43-51.
33. Ohshiro, T., Matsuda, D., Sakai, K., et al. (2011). Pyripyropene A, an acylcoenzyme A:cholesterol acyltransferase 2-selective inhibitor, attenuates hypercholesterolemia and atherosclerosis in murine models of hyperlipidemia. Arterioscler. Thromb. Vasc. Biol. 31, 1108-1115.
34. Panini, S.R., and Sinensky, M.S. (2001). Mechanisms of oxysterol-induced apoptosis. Curr. Opin. Lipidol. 12, 529-533.
35. Parini, P., Davis, M., Lada, A.T., et al. (2004). ACAT2 is localized to hepatocytes and is the major cholesterol-esterifying enzyme in human liver. Circulation 110, 2017-2023.
36. Parkin, D.M., Bray, F., Ferlay, J., et al. (2005). Global cancer statistics, 2002. CA Cancer J. Clin. 55, 74-108.
37. Pramfalk, C., Davis, M.A., Eriksson, M., et al. (2005). Control of ACAT2 liver expression by HNF1. J. Lipid Res. 46, 1868-1876.
38. Repa, J.J., Buhman, K.K., Farese, R.V., et al. (2004). ACAT2 deficiency limits cholesterol absorption in the cholesterol-fed mouse: impact on hepatic cholesterol homeostasis. Hepatology 40, 1088-1097.
39. Rothblat, G.H., and Phillips, M.C. (2010). High-density lipoprotein heterogeneity and function in reverse cholesterol transport. Curr. Opin. Lipidol. 21, 229-238.
40. Rusinol, A.E., Thewke, D., Liu, J., et al. (2004). AKT/protein kinase B regulation of BCL family members during oxysterol-induced apoptosis. J. Biol. Chem. 279, 1392-1399.
41. Russell, D.W. (2003). The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72, 137-174.
42. Schroepfer, G.J., Jr (2000). Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 80, 361-554.
43. Smith, J.L., Rangaraj, K., Simpson, R., et al. (2004). Quantitative analysis of the expression of ACAT genes in human tissues by real-time PCR. J. Lipid Res. 45, 686-696.
44. Song, B.L., Qi, W., Yang, X.Y., et al. (2001). Organization of human ACAT-2 gene and its cell-type-specific promoter activity. Biochem. Biophys. Res. Commun. 282, 580-588.
45. Song, B.L., Wang, C.H., Yao, X.M., et al. (2006). Humanacyl-CoA: cholesterol acyltransferase 2 gene expression in intestinal Caco-2 cells and in hepatocellular carcinoma. Biochem. J. 394, 617-626.
46. Struhl, K. (1998). Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 12, 599-606.
47. Sundaram, M., and Yao, Z. (2010). Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr. Metab. (Lond) 7, 35.
48. Tardif, J.C., Gregoire, J., L'Allier, P.L., et al. (2004). Effects of the acyl coenzyme A:cholesterol acyltransferase inhibitor avasimibe on human atherosclerotic lesions. Circulation 110, 3372-3377.
49. Tennant, D.A., Duran, R.V., Boulahbel, H., et al. (2009). Metabolic transformation in cancer. Carcinogenesis 30, 1269-1280.
50. Tennant, D.A., Duran, R.V., and Gottlieb, E. (2010). Targeting metabolic transformation for cancer therapy. Nat. Rev. Cancer 10, 267-277.
51. Wu, J.M., Skill, N.J., and Maluccio, M.A. (2010). Evidence of aberrant lipid metabolism in hepatitis C and hepatocellular carcinoma. HPB (Oxford) 12, 625-636.