Regulation of lipogenic gene expression by lysine-specific histone demethylase-1 (LSD1)

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 29937-29947

  Abdulla, Arian ^a   Zhang, Yi ^a   Hsu, Fu Ning ^b   Xiaoli, Alus M ^a   Zhao, Xiaoping ^a   Yang, Ellen S T ^a   Ji, Jun Yuan ^b   Yang, Fajun ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; FATTY ACIDS; MAMMALS; METABOLISM; PHYSIOLOGY; PROTEINS; TRANSCRIPTION;

CARDIO-VASCULAR DISEASE; HISTONE DEACETYLASES; HISTONE DEMETHYLASE LSD1; REGULATORY MECHANISM; STEROL REGULATORY ELEMENT-BINDING PROTEINS; TRANSCRIPTION LEVEL; TRANSCRIPTIONAL ACTIVATORS; TRIGLYCERIDE LEVELS;

GENE EXPRESSION REGULATION;

HISTONE DEMETHYLASE; LYSINE SPECIFIC HISTONE DEMETHYLASE 1; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; FATTY ACID SYNTHASE; KDM1A PROTEIN, HUMAN; PROTEIN BINDING; SIRT1 PROTEIN, HUMAN; SIRTUIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; FAS GENE; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LIPID METABOLISM; LIVER CELL; LSD1 GENE; MALE; MOUSE; NONHUMAN; PROMOTER REGION; SIRT1 GENE; SREBP1 GENE; ANIMAL; CELL NUCLEUS; GENETICS; HEK293 CELL LINE; HEPG2 CELL LINE; LIPOGENESIS; METABOLISM;

ANIMALS; CELL NUCLEUS; FATTY ACID SYNTHASES; GENE EXPRESSION REGULATION; HEK293 CELLS; HEP G2 CELLS; HEPATOCYTES; HISTONE DEMETHYLASES; HUMANS; LIPOGENESIS; MALE; MICE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIRTUIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION, GENETIC;

EID: 84908439685     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.573659     Document Type: Article

References (51)

1. Osborne, T. F., and Espenshade, P. J. (2009) Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been. Genes Dev. 23, 2578-2591
2. Jeon, T. I., and Osborne, T. F. (2012) SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol. Metab. 23, 65-72
3. Xiaoli, and Yang, F. (2013) Mediating lipid biosynthesis: Implications for cardiovascular disease. Trends Cardiovasc. Med. 23, 269-273
4. Shimomura, I., Shimano, H., Horton, J. D., Goldstein, J. L., and Brown, M. S. (1997) Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. J. Clin. Invest. 99, 838-845
5. Im, S. S., Yousef, L., Blaschitz, C., Liu, J. Z., Edwards, R. A., Young, S. G., Raffatellu, M., and Osborne, T. F. (2011) Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab. 13, 540-549
6. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131
7. Hua, X., Yokoyama, C., Wu, J., Briggs, M. R., Brown, M. S., Goldstein, J. L., and Wang, X. (1993) SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proc. Natl. Acad. Sci. U.S.A. 90, 11603-11607
8. Yokoyama, C., Wang, X., Briggs, M. R., Admon, A., Wu, J., Hua, X., Goldstein, J. L., and Brown, M. S. (1993) SREBP-1, a basic-helix-loop-helix-leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 75, 187-197
9. Wang, X., Sato, R., Brown, M. S., Hua, X., and Goldstein, J. L. (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 77, 53-62
10. Amemiya-Kudo, M., Shimano, H., Hasty, A. H., Yahagi, N., Yoshikawa, T., Matsuzaka, T., Okazaki, H., Tamura, Y., Iizuka, Y., Ohashi, K., Osuga, J., Harada, K., Gotoda, T., Sato, R., Kimura, S., Ishibashi, S., and Yamada, N. (2002) Transcriptional activities of nuclear SREBP-1a, -1c, and -2 to different target promoters of lipogenic and cholesterogenic genes. J. Lipid Res. 43, 1220-1235
11. Zhang, Y., Xiaoli, Zhao, X., and Yang, F. (2013) The mediator complex and lipid metabolism. J. Biochem. Pharmacol. Res. 1, 51-55
12. Giandomenico, V., Simonsson, M., Grönroos, E., and Ericsson, J. (2003) Coactivator-dependent acetylation stabilizes members of the SREBP family of transcription factors. Mol. Cell. Biol. 23, 2587-2599
13. Näär, A. M., Beaurang, P. A., Zhou, S., Abraham, S., Solomon, W., and Tjian, R. (1999) Composite co-activator ARC mediates chromatin-directed transcriptional activation. Nature 398, 828-832
14. Yang, F., Vought, B. W., Satterlee, J. S., Walker, A. K., Jim Sun, Z. Y., Watts, J. L., DeBeaumont, R., Saito, R. M., Hyberts, S. G., Yang, S., Macol, C., Iyer, L., Tjian, R., van den Heuvel, S., Hart, A. C., Wagner, G., and Näär, A. M. (2006) An ARC/mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442, 700-704
15. Sundqvist, A., Bengoechea-Alonso, M. T., Ye, X., Lukiyanchuk, V., Jin, J., Harper, J. W., and Ericsson, J. (2005) Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metab. 1, 379-391
16. Bengoechea-Alonso, M. T., and Ericsson, J. (2009) A phosphorylation cascade controls the degradation of active SREBP1. J. Biol. Chem. 284, 5885-5895
17. Zhao, X., Feng, D., Wang, Q., Abdulla, A., Xie, X. J., Zhou, J., Sun, Y., Yang, E. S., Liu, L. P., Vaitheesvaran, B., Bridges, L., Kurland, I. J., Strich, R., Ni, J. Q., Wang, C., Ericsson, J., Pessin, J. E., Ji, J. Y., and Yang, F. (2012) Regulation of lipogenesis by cyclin-dependent kinase 8-mediated control of SREBP-1. J. Clin. Invest. 122, 2417-2427
18. Shaw, M., Cohen, P., and Alessi, D. R. (1997) Further evidence that the inhibition of glycogen synthase kinase-3beta by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216. FEBS Lett. 416, 307-311
19. Chang, H. C., and Guarente, L. (2014) SIRT1 and other sirtuins in metabolism. Trends Endocrinol. Metab. 25, 138-145
20. Walker, A. K., Yang, F., Jiang, K., Ji, J. Y., Watts, J. L., Purushotham, A., Boss, O., Hirsch, M. L., Ribich, S., Smith, J. J., Israelian, K., Westphal, C. H., Rodgers, J. T., Shioda, T., Elson, S. L., Mulligan, P., Najafi-Shoushtari, H., Black, J. C., Thakur, J. K., Kadyk, L. C., Whetstine, J. R., Mostoslavsky, R., Puigserver, P., Li, X., Dyson, N. J., Hart, A. C., and Näär, A. M. (2010) Conserved role of SIRT1 orthologs in fasting-dependent inhibition of the lipid/cholesterol regulator SREBP. Genes Dev. 24, 1403-1417
21. You, M., Liang, X., Ajmo, J. M., and Ness, G. C. (2008) Involvement of mammalian sirtuin 1 in the action of ethanol in the liver. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G892-G898
22. Ponugoti, B., Kim, D. H., Xiao, Z., Smith, Z., Miao, J., Zang, M., Wu, S. Y., Chiang, C. M., Veenstra, T. D., and Kemper, J. K. (2010) SIRT1 deacetylates and inhibits SREBP-1C activity in regulation of hepatic lipid metabolism. J. Biol. Chem. 285, 33959-33970
23. Rodgers, J. T., and Puigserver, P. (2007) Fasting-dependent glucose and lipid metabolic response through hepatic sirtuin 1. Proc. Natl. Acad. Sci. U.S.A. 104, 12861-12866
24. Erion, D. M., Yonemitsu, S., Nie, Y., Nagai, Y., Gillum, M. P., Hsiao, J. J., Iwasaki, T., Stark, R., Weismann, D., Yu, X. X., Murray, S. F., Bhanot, S., Monia, B. P., Horvath, T. L., Gao, Q., Samuel, V. T., and Shulman, G. I. (2009) SirT1 knockdown in liver decreases basal hepatic glucose production and increases hepatic insulin responsiveness in diabetic rats. Proc. Natl. Acad. Sci. U.S.A. 106, 11288-11293
25. Li, X., Zhang, S., Blander, G., Tse, J. G., Krieger, M., and Guarente, L. (2007) SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell 28, 91-106
26. Pfluger, P. T., Herranz, D., Velasco-Miguel, S., Serrano, M., and Tschöp, M. H. (2008) Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. U.S.A. 105, 9793-9798
27. Purushotham, A., Schug, T. T., Xu, Q., Surapureddi, S., Guo, X., and Li, X. (2009) Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 9, 327-338
28. Mulligan, P., Yang, F., Di Stefano, L., Ji, J. Y., Ouyang, J., Nishikawa, J. L., Toiber, D., Kulkarni, M., Wang, Q., Najafi-Shoushtari, S. H., Mostoslavsky, R., Gygi, S. P., Gill, G., Dyson, N. J., and Näär, A. M. (2011) A SIRT1-LSD1 corepressor complex regulates Notch target gene expression and development. Mol. Cell 42, 689-699
29. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., and Casero, R. A. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953
30. Metzger, E., Wissmann, M., Yin, N., Müller, J. M., Schneider, R., Peters, A. H., Günther, T., Buettner, R., and Schüle, R. (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437, 436-439
31. Garcia-Bassets, I., Kwon, Y. S., Telese, F., Prefontaine, G. G., Hutt, K. R., Cheng, C. S., Ju, B. G., Ohgi, K. A., Wang, J., Escoubet-Lozach, L., Rose, D. W., Glass, C. K., Fu, X. D., and Rosenfeld, M. G. (2007) Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128, 505-518
32. Huang, J., Sengupta, R., Espejo, A. B., Lee, M. G., Dorsey, J. A., Richter, M., Opravil, S., Shiekhattar, R., Bedford, M. T., Jenuwein, T., and Berger, S. L. (2007) p53 is regulated by the lysine demethylase LSD1. Nature 449, 105-108
33. Wang, J., Hevi, S., Kurash, J. K., Lei, H., Gay, F., Bajko, J., Su, H., Sun, W., Chang, H., Xu, G., Gaudet, F., Li, E., and Chen, T. (2009) The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat. Genet. 41, 125-129
34. Shi, Y., Sawada, J., Sui, G., Affarel, B., Whetstine, J. R., Lan, F., Ogawa, H., Luke, M. P., and Nakatani, Y. (2003) Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735-738
35. Lee, M. G., Wynder, C., Cooch, N., and Shiekhattar, R. (2005) An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432-435
36. Forneris, F., Binda, C., Battaglioli, E., and Mattevi, A. (2008) LSD1: oxidative chemistry for multifaceted functions in chromatin regulation. Trends Biochem. Sci. 33, 181-189
37. Hino, S., Sakamoto, A., Nagaoka, K., Anan, K., Wang, Y., Mimasu, S., Umehara, T., Yokoyama, S., Kosai, K., and Nakao, M. (2012) FAD-dependent lysine-specific demethylase-1 regulates cellular energy expenditure. Nat. Commun. 3, 758
38. Musri, M. M., Carmona, M. C., Hanzu, F. A., Kaliman, P., Gomis, R., and Párrizas, M. (2010) Histone demethylase LSD1 regulates adipogenesis. J. Biol. Chem. 285, 30034-30041
39. Zhang, C., Shin, D. J., and Osborne, T. F. (2005) A simple promoter containing two Sp1 sites controls the expression of sterol-regulatory-element-binding protein 1a (SREBP-1a). Biochem. J. 386, 161-168
40. Dif, N., Euthine, V., Gonnet, E., Laville, M., Vidal, H., and Lefai, E. (2006) Insulin activates human sterol-regulatory-element-binding protein-1c (SREBP-1c) promoter through SRE motifs. Biochem. J. 400, 179-188
41. Castoreno, A. B., Wang, Y., Stockinger, W., Jarzylo, L. A., Du, H., Pagnon, J. C., Shieh, E. C., and Nohturfft, A. (2005) Transcriptional regulation of phagocytosis-induced membrane biogenesis by sterol regulatory element binding proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 13129-13134
42. Stavropoulos, P., Blobel, G., and Hoelz, A. (2006) Crystal structure and mechanism of human lysine-specific demethylase-1. Nat. Struct. Mol. Biol. 13, 626-632
43. Hua, X., Wu, J., Goldstein, J. L., Brown, M. S., and Hobbs, H. H. (1995) Structure of the human gene encoding sterol regulatory element binding protein-1 (SREBF1) and localization of SREBF1 and SREBF2 to chromosomes 17p11.2 and 22q13. Genomics 25, 667-673
44. Lee, M. G., Wynder, C., Schmidt, D. M., McCafferty, D. G., and Shiekhattar, R. (2006) Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chem. Biol. 13, 563-567
45. Abdulla, A., Zhao, X., and Yang, F. (2013) Natural polyphenols inhibit lysine-specific demethylase-1. J. Biochem. Pharmacol. Res. 1, 56-63
46. Baur, J. A., Pearson, K. J., Price, N. L., Jamieson, H. A., Lerin, C., Kalra, A., Prabhu, V. V., Allard, J. S., Lopez-Lluch, G., Lewis, K., Pistell, P. J., Poosala, S., Becker, K. G., Boss, O., Gwinn, D., Wang, M., Ramaswamy, S., Fishbein, K. W., Spencer, R. G., Lakatta, E. G., Le Couteur, D., Shaw, R. J., Navas, P., Puigserver, P., Ingram, D. K., de Cabo, R., and Sinclair, D. A. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444, 337-342
47. Zingg, J. M., Hasan, S. T., and Meydani, M. (2013) Molecular mechanisms of hypolipidemic effects of curcumin. Biofactors 39, 101-121
48. Boots, A. W., Haenen, G. R., and Bast, A. (2008) Health effects of quercetin: from antioxidant to nutraceutical. Eur. J. Pharmacol. 585, 325-337
49. Hannah, V. C., Ou, J., Luong, A., Goldstein, J. L., and Brown, M. S. (2001) Unsaturated fatty acids down-regulate srebp isoforms 1a and 1c by two mechanisms in HEK-293 cells. J. Biol. Chem. 276, 4365-4372
50. Chuang, J. Y., Chang, W. C., and Hung, J. J. (2011) Hydrogen peroxide induces Sp1 methylation and thereby suppresses cyclin B1 via recruitment of Suv39H1 and HDAC1 in cancer cells. Free Radic. Biol. Med. 51, 2309-2318
51. Choi, W. I., Jeon, B. N., Park, H., Yoo, J. Y., Kim, Y. S., Koh, D. I., Kim, M. H., Kim, Y. R., Lee, C. E., Kim, K. S., Osborne, T. F., and Hur, M. W. (2008) Proto-oncogene FBI-1 (Pokemon) and SREBP-1 synergistically activate transcription of fatty-acid synthase gene (FASN). J. Biol. Chem. 283, 29341-29354