Inhibition of ATP citrate lyase induces triglyceride accumulation with altered fatty acid composition in cancer cells

International Journal of Cancer

Volumn 135, Issue 1, 2014, Pages 37-47

  Migita, Toshiro ^a,b   Okabe, Sachiko ^a   Ikeda, Kazutaka ^c,d   Igarashi, Saori ^d   Sugawara, Shoko ^d   Tomida, Akihiro ^a   Soga, Tomoyoshi ^d   Taguchi, Ryo ^c,e   Seimiya, Hiroyuki ^a  

^a CANCER CHEMOTHERAPY CENTER   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d KEIO UNIVERSITY   (Japan)

^e CHUBU UNIVERSITY   (Japan)

Author keywords

ATP citrate lyase; carnitine palmitoyltransferase 1; elongation of long chain fatty acids family member 6

Indexed keywords

ATP CITRATE LYASE; CARNITINE PALMITOYLTRANSFERASE 1; ELONGATION OF LONG-CHAIN FATTY ACIDS FAMILY MEMBER 6;

ACETYLTRANSFERASES; ATP CITRATE (PRO-S)-LYASE; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; FATTY ACIDS; HUMANS; LIPID METABOLISM; MITOCHONDRIA; NEOPLASMS; TRIGLYCERIDES;

EID: 84899441699     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28652     Document Type: Article

References (48)

1. Rysman E, Brusselmans K, Scheys K, et al. De novo lipogenesis protects cancer cells from free radicals and chemotherapeutics by promoting membrane lipid saturation. Cancer Res 2000; 70: 8117-26.
2. Fiorentino M, Zadra G, Palescandolo E, et al. Overexpression of fatty acid synthase is associated with palmitoylation of Wnt1 and cytoplasmic stabilization of beta-catenin in prostate cancer. Lab Invest 2008; 88: 1340-8.
3. Migita T, Ruiz S, Fornari A, et al. Fatty acid synthase: a metabolic enzyme and candidate oncogene in prostate cancer. J Natl Cancer Inst 2009; 101: 519-32.
4. Baron A, Migita T, Tang D, et al. Fatty acid synthase: a metabolic oncogene in prostate cancer? J Cell Biochem 2004; 91: 47-53.
5. Menendez JA, Lupu R,. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 2007; 7: 763-77.
6. Zaugg K, Yao Y, Reilly PT, et al. Carnitine palmitoyltransferase 1C promotes cell survival and tumor growth under conditions of metabolic stress. Genes Dev 2011; 25: 1041-51.
7. Carracedo A, Cantley LC, Pandolfi PP,. Cancer metabolism: fatty acid oxidation in the limelight. Nat Rev Cancer 2013; 13: 227-32.
8. Bauer DE, Hatzivassiliou G, Zhao F, et al. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005; 24: 6314-22.
9. Beckner ME, Fellows-Mayle W, Zhang Z, et al. Identification of ATP citrate lyase as a positive regulator of glycolytic function in glioblastomas. Int J Cancer 126: 2282-95.
10. Hatzivassiliou G, Zhao F, Bauer DE, et al. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 2005; 8: 311-21.
11. Migita T, Narita T, Nomura K, et al. ATP citrate lyase: activation and therapeutic implications in non-small cell lung cancer. Cancer Res 2008; 68: 8547-54.
12. Schwartz L, Abolhassani M, Guais A, et al. A combination of alpha lipoic acid and calcium hydroxycitrate is efficient against mouse cancer models: preliminary results. Oncol Rep 2010; 23: 1407-16.
13. Zaidi N, Royaux I, Swinnen JV, et al. ATP citrate lyase knockdown induces growth arrest and apoptosis through different cell- and environment-dependent mechanisms. Mol Cancer Ther 2012; 11: 1925-35.
14. Zaidi N, Swinnen JV, Smans K,. ATP-citrate lyase: a key player in cancer metabolism. Cancer Res 2012; 72: 3709-14.
15. Migita T, Okabe S, Ikeda K, et al. Inhibition of ATP citrate lyase induces an anticancer effect via reactive oxygen species: AMPK as a predictive biomarker for therapeutic impact. Am J Pathol 2013; 182: 1800-10.
16. Mashima T, Oh-hara T, Sato S, et al. p53-defective tumors with a functional apoptosome-mediated pathway: a new therapeutic target. J Natl Cancer Inst 2005; 97: 765-77.
17. Bligh EG, Dyer WJ,. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911-7.
18. Ikeda K, Mutoh M, Teraoka N, et al. Increase of oxidant-related triglycerides and phosphatidylcholines in serum and small intestinal mucosa during development of intestinal polyp formation in Min mice. Cancer Sci 2011; 102: 79-87.
19. Soga T, Baran R, Suematsu M, et al. Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. J Biol Chem 2006; 281: 16768-76.
20. Green CD, Ozguden-Akkoc CG, Wang Y, et al. Role of fatty acid elongases in determination of de novo synthesized monounsaturated fatty acid species. J Lipid Res 2010; 51: 1871-7.
21. Guillou H, Zadravec D, Martin PG, et al. The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Prog Lipid Res 2010; 49: 186-99.
22. Matsuzaka T, Shimano H,. Elovl6: a new player in fatty acid metabolism and insulin sensitivity. J Mol Med 2009; 87: 379-84.
23. Jakobsson A, Westerberg R, Jacobsson A,. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 2006; 45: 237-49.
24. Matsuzaka T, Shimano H, Yahagi N, et al. Crucial role of a long-chain fatty acid elongase, Elovl6, in obesity-induced insulin resistance. Nat Med 2007; 13: 1193-202.
25. Pazouki S, Baty JD, Wallace HM, et al. Utilization of extracellular lipids by HT29/219 cancer cells in culture. Lipids 1992; 27: 827-34.
26. Kuhajda FP,. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition 2000; 16: 202-8.
27. Ookhtens M, Kannan R, Lyon I, et al. Liver and adipose tissue contributions to newly formed fatty acids in an ascites tumor. Am J Physiol 1984; 247: R146-53.
28. Swinnen JV, Brusselmans K, Verhoeven G,. Increased lipogenesis in cancer cells: new players, novel targets. Curr Opin Clin Nutr Metab Care 2006; 9: 358-65.
29. Mashima T, Seimiya H, Tsuruo T,. De novo fatty-acid synthesis and related pathways as molecular targets for cancer therapy. Br J Cancer 2009; 100: 1369-72.
30. Abramson HN,. The lipogenesis pathway as a cancer target. J Med Chem 2011; 54: 5615-38.
31. Zu XY, Zhang QH, Liu JH, et al. ATP citrate lyase inhibitors as novel cancer therapeutic agents. Recent Pat Anticancer Drug Discov 2012; 7: 154-67.
32. Chu KY, Lin Y, Hendel A, et al. ATP-citrate lyase reduction mediates palmitate-induced apoptosis in pancreatic beta cells. J Biol Chem; 285: 32606-15.
33. Wellen KE, Hatzivassiliou G, Sachdeva UM, et al. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009; 324: 1076-80.
34. Wang Q, Jiang L, Wang J, et al. Abrogation of hepatic ATP-citrate lyase protects against fatty liver and ameliorates hyperglycemia in leptin receptor-deficient mice. Hepatology 2009; 49: 1166-75.
35. Tamura K, Makino A, Hullin-Matsuda F, et al. Novel lipogenic enzyme ELOVL7 is involved in prostate cancer growth through saturated long-chain fatty acid metabolism. Cancer Res 2009; 69: 8133-40.
36. Matsuzaka T, Atsumi A, Matsumori R, et al. Elovl6 promotes nonalcoholic steatohepatitis. Hepatology 2012; 56: 2199-208.
37. Muir K, Hazim A, He Y, et al. Proteomic and lipidomic signatures of lipid metabolism in NASH-associated hepatocellular carcinoma. Cancer Res 2013; 73: 4722-31.
38. Jump DB, Torres-Gonzalez M, Olson LK,. Soraphen A, an inhibitor of acetyl CoA carboxylase activity, interferes with fatty acid elongation. Biochem Pharmacol 2011; 81: 649-60.
39. Hapala I, Marza E, Ferreira T,. Is fat so bad? Modulation of endoplasmic reticulum stress by lipid droplet formation. Biol Cell 2011; 103: 271-85.
40. Schaffer JE,. Lipotoxicity: When tissues overeat. Curr Opin Lipidol 2003; 14: 281-7.
41. Listenberger LL, Han X, Lewis SE, et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 2003; 100: 3077-82.
42. Cnop M, Hannaert JC, Hoorens A, et al. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001; 50: 1771-7.
43. Maedler K, Spinas GA, Dyntar D, et al. Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 2001; 50: 69-76.
44. Hardy S, Langelier Y, Prentki M,. Oleate activates phosphatidylinositol 3-kinase and promotes proliferation and reduces apoptosis of MDA-MB-231 breast cancer cells, whereas palmitate has opposite effects. Cancer Res 2000; 60: 6353-8.
45. Hardy S, El-Assaad W, Przybytkowski E, et al. Saturated fatty acid-induced apoptosis in MDA-MB-231 breast cancer cells. A role for cardiolipin. J Biol Chem 2003; 278: 31861-70.
46. Swinnen JV, Van Veldhoven PP, Timmermans L, et al. Fatty acid synthase drives the synthesis of phospholipids partitioning into detergent-resistant membrane microdomains. Biochem Biophys Res Commun 2003; 302: 898-903.
47. Zhou W, Simpson PJ, McFadden JM, et al. Fatty acid synthase inhibition triggers apoptosis during S phase in human cancer cells. Cancer Res 2003; 63: 7330-7.
48. Wang Q, Li S, Jiang L, et al. Deficiency in hepatic ATP-citrate lyase affects VLDL-triglyceride mobilization and liver fatty acid composition in mice. J Lipid Res; 51: 2516-26.