Acetylation stabilizes ATP-citrate lyase to promote lipid biosynthesis and tumor growth

Molecular Cell

Volumn 51, Issue 4, 2013, Pages 506-518

  Lin, Ruiting ^a,b   Tao, Ren ^c   Gao, Xue ^a,b   Li, Tingting ^a,b   Zhou, Xin ^a,b   Guan, Kun Liang ^a,d   Xiong, Yue ^a,b,e   Lei, Qun Ying ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE CITRATE LYASE; CALCIUM BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; FATTY ACID; GLUCOSE; SIRTUIN 2;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DEACETYLATION; ENZYMATIC DEGRADATION; ENZYME STABILITY; FATTY ACID SYNTHESIS; HUMAN; HUMAN TISSUE; LUNG CANCER; MALE; MOUSE; NONHUMAN; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ACETYLATION; ANIMALS; ATP CITRATE (PRO-S)-LYASE; BLOTTING, WESTERN; CALMODULIN-BINDING PROTEINS; CELL PROLIFERATION; CYTOSKELETAL PROTEINS; FATTY ACIDS; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; P300-CBP TRANSCRIPTION FACTORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIRTUIN 2; TUMOR CELLS, CULTURED; UBIQUITIN; UBIQUITINATION;

EID: 84882605310     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.07.002     Document Type: Article

References (36)

1. Bauer D.E., Hatzivassiliou G., Zhao F., Andreadis C., Thompson C.B. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005, 24:6314-6322.
2. Berwick D.C., Hers I., Heesom K.J., Moule S.K., Tavare J.M. The identification of ATP-citrate lyase as a protein kinase B (Akt) substrate in primary adipocytes. J.Biol. Chem. 2002, 277:33895-33900.
3. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
4. Grönroos E., Hellman U., Heldin C.H., Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol. Cell 2002, 10:483-493.
5. Hamar P., Song E., Kökény G., Chen A., Ouyang N., Lieberman J. Small interfering RNA targeting Fas protects mice against renal ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA 2004, 101:14883-14888.
6. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
7. Hatzivassiliou G., Zhao F., Bauer D.E., Andreadis C., Shaw A.N., Dhanak D., Hingorani S.R., Tuveson D.A., Thompson C.B. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 2005, 8:311-321.
8. Icard P., Poulain L., Lincet H. Understanding the central role of citrate in the metabolism of cancer cells. Biochim. Biophys. Acta 2012, 1825:111-116.
9. Jiang W., Wang S., Xiao M., Lin Y., Zhou L., Lei Q., Xiong Y., Guan K.L., Zhao S. Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase. Mol. Cell 2011, 43:33-44.
10. Kim Y.M., Shin H.T., Seo Y.H., Byun H.O., Yoon S.H., Lee I.K., Hyun D.H., Chung H.Y., Yoon G. Sterol regulatory element-binding protein (SREBP)-1-mediated lipogenesis is involved in cell senescence. J.Biol. Chem. 2010, 285:29069-29077.
11. Kuhajda F.P. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition 2000, 16:202-208.
12. Lara E., Mai A., Calvanese V., Altucci L., Lopez-Nieva P., Martinez-Chantar M.L., Varela-Rey M., Rotili D., Nebbioso A., Ropero S., et al. Salermide, a Sirtuin inhibitor with a strong cancer-specific proapoptotic effect. Oncogene 2009, 28:781-791.
13. Lei Q., Jiao J., Xin L., Chang C.J., Wang S., Gao J., Gleave M.E., Witte O.N., Liu X., Wu H. NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer Cell 2006, 9:367-378.
14. Li M., Luo J., Brooks C.L., Gu W. Acetylation of p53 inhibits its ubiquitination by Mdm2. J.Biol. Chem. 2002, 277:50607-50611.
15. Li H., Wittwer T., Weber A., Schneider H., Moreno R., Maine G.N., Kracht M., Schmitz M.L., Burstein E. Regulation of NF-κB activity by competition between RelA acetylation and ubiquitination. Oncogene 2012, 31:611-623.
16. McAndrew P.F. Fat metabolism and cancer. Surg. Clin. North Am. 1986, 66:1003-1012.
17. Medes G., Thomas A., Weinhouse S. Metabolism of neoplastic tissue. IV. A study of lipid synthesis in neoplastic tissue slices invitro. Cancer Res. 1953, 13:27-29.
18. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 2007, 7:763-777.
19. Migita T., Narita T., Nomura K., Miyagi E., Inazuka F., Matsuura M., Ushijima M., Mashima T., Seimiya H., Satoh Y., et al. ATP citrate lyase: activation and therapeutic implications in non-small cell lung cancer. Cancer Res. 2008, 68:8547-8554.
20. Milgraum L.Z., Witters L.A., Pasternack G.R., Kuhajda F.P. Enzymes of the fatty acid synthesis pathway are highly expressed in insitu breast carcinoma. Clin. Cancer Res. 1997, 3:2115-2120.
21. Nadler S.T., Stoehr J.P., Rabaglia M.E., Schueler K.L., Birnbaum M.J., Attie A.D. Normal Akt/PKB with reduced PI3K activation in insulin-resistant mice. Am. J. Physiol. Endocrinol. Metab. 2001, 281:E1249-E1254.
22. Ookhtens M., Kannan R., Lyon I., Baker N. Liver and adipose tissue contributions to newly formed fatty acids in an ascites tumor. Am. J. Physiol. 1984, 247:R146-R153.
23. Pierce M.W., Palmer J.L., Keutmann H.T., Hall T.A., Avruch J. The insulin-directed phosphorylation site on ATP-citrate lyase is identical with the site phosphorylated by the cAMP-dependent protein kinase invitro. J.Biol. Chem. 1982, 257:10681-10686.
24. Potapova I.A., El-Maghrabi M.R., Doronin S.V., Benjamin W.B. Phosphorylation of recombinant human ATP:citrate lyase by cAMP-dependent protein kinase abolishes homotropic allosteric regulation of the enzyme by citrate and increases the enzyme activity. Allosteric activation of ATP:citrate lyase by phosphorylated sugars. Biochemistry 2000, 39:1169-1179.
25. Rysman E., Brusselmans K., Scheys K., Timmermans L., Derua R., Munck S., Van Veldhoven P.P., Waltregny D., Daniëls V.W., Machiels J., et al. De novo lipogenesis protects cancer cells from free radicals and chemotherapeutics by promoting membrane lipid saturation. Cancer Res. 2010, 70:8117-8126.
26. Sabine J.R., Abraham S., Chaikoff I.L. Control of lipid metabolism in hepatomas: insensitivity of rate of fatty acid and cholesterol synthesis by mouse hepatoma BW7756 to fasting and to feedback control. Cancer Res. 1967, 27:793-799.
27. Swinnen J.V., Heemers H., van de Sande T., de Schrijver E., Brusselmans K., Heyns W., Verhoeven G. Androgens, lipogenesis and prostate cancer. J.Steroid Biochem. Mol. Biol. 2004, 92:273-279.
28. Swinnen J.V., Brusselmans K., Verhoeven G. Increased lipogenesis in cancer cells: new players, novel targets. Curr. Opin. Clin. Nutr. Metab. Care 2006, 9:358-365.
29. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
30. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., Choudhary C. A proteome-wide, quantitative survey of invivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 2011, 10. M111, 013284.
31. Wang H., Dey S.K. Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 2006, 7:185-199.
32. Wellen K.E., Hatzivassiliou G., Sachdeva U.M., Bui T.V., Cross J.R., Thompson C.B. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080.
33. Yahagi N., Shimano H., Hasegawa K., Ohashi K., Matsuzaka T., Najima Y., Sekiya M., Tomita S., Okazaki H., Tamura Y., et al. Co-ordinate activation of lipogenic enzymes in hepatocellular carcinoma. Eur. J. Cancer 2005, 41:1316-1322.
34. Zaidi N., Royaux I., Swinnen J.V., Smans K. ATP citrate lyase knockdown induces growth arrest and apoptosis through different cell- and environment-dependent mechanisms. Mol. Cancer Ther. 2012, 11:1925-1935.
35. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., Yao J., Zhou L., Zeng Y., Li H., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.
36. Zu X.Y., Zhang Q.H., Liu J.H., Cao R.X., Zhong J., Yi G.H., Quan Z.H., Pizzorno G. ATP citrate lyase inhibitors as novel cancer therapeutic agents. Recent Patents Anticancer. Drug Discov. 2012, 7:154-167.