SETDB2 Links Glucocorticoid to Lipid Metabolism through Insig2a Regulation

Cell Metabolism

Volumn 24, Issue 3, 2016, Pages 474-484

  Roqueta Rivera, Manuel ^a   Esquejo, Ryan M ^a   Phelan, Peter E ^a   Sandor, Katalin ^a   Daniel, Bence ^a   Foufelle, Fabienne ^b,c   Ding, Jun ^d   Li, Xiaoman ^d   Khorasanizadeh, Sepideh ^a   Osborne, Timothy F ^a  

^a BURNHAM INSTITUTE   (United States)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

fasting liver; glucocorticoid receptor; insig2; SETDB2; SREBP

Indexed keywords

FATTY ACID; GLUCOCORTICOID; INSIG2 PROTEIN; LIPID; MESSENGER RNA; REGULATOR PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG; CHROMATIN; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; INSIG2 PROTEIN, MOUSE; LYSINE; MEMBRANE PROTEIN; PROTEIN BINDING; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ADENOVIRIDAE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CHROMATIN; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID OXIDATION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE LOCUS; LIPID METABOLISM; LIPOGENESIS; LIVER; LIVER CELL; MODIFIER GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METHYLATION; REFEEDING; RNA SEQUENCE; SETDB2 GENE; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENHANCER REGION; FEEDING BEHAVIOR; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM; METHYLATION; MOUSE MUTANT; PROMOTER REGION;

ANIMALS; CHROMATIN; DEXAMETHASONE; ENHANCER ELEMENTS, GENETIC; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC LOCI; GLUCOCORTICOIDS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LIPID METABOLISM; LIVER; LYSINE; MALE; MEMBRANE PROTEINS; METHYLATION; MICE, INBRED C57BL; MICE, OBESE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION, GENETIC;

EID: 84990851590     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.07.025     Document Type: Article

References (47)

1. Abe, Y., Rozqie, R., Matsumura, Y., Kawamura, T., Nakaki, R., Tsurutani, Y., Tanimura-Inagaki, K., Shiono, A., Magoori, K., Nakamura, K., et al. JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis. Nat. Commun., 6, 2015, 7052.
2. Ahmed, A., Rabbitt, E., Brady, T., Brown, C., Guest, P., Bujalska, I.J., Doig, C., Newsome, P.N., Hubscher, S., Elias, E., et al. A switch in hepatic cortisol metabolism across the spectrum of non alcoholic fatty liver disease. PLoS ONE, 7, 2012, e29531.
3. Alam, H., Gu, B., Lee, M.G., Histone methylation modifiers in cellular signaling pathways. Cell. Mol. Life Sci. 72 (2015), 4577–4592.
4. Biggar, K.K., Li, S.S., Non-histone protein methylation as a regulator of cellular signalling and function. Nat. Rev. Mol. Cell Biol. 16 (2015), 5–17.
5. Binda, O., Boyce, M., Rush, J.S., Palaniappan, K.K., Bertozzi, C.R., Gozani, O., A chemical method for labeling lysine methyltransferase substrates. ChemBioChem 12 (2011), 330–334.
6. Bittencourt, D., Wu, D.Y., Jeong, K.W., Gerke, D.S., Herviou, L., Ianculescu, I., Chodankar, R., Siegmund, K.D., Stallcup, M.R., G9a functions as a molecular scaffold for assembly of transcriptional coactivators on a subset of glucocorticoid receptor target genes. Proc. Natl. Acad. Sci. USA 109 (2012), 19673–19678.
7. Blake, R.L., Hydrocortisone induction of tyrosine aminotransferase activity in genetically obese and diabetic mice—effects of a multiple dosage schedule. Biochem. Pharmacol. 19 (1970), 1508–1512.
8. Blake, R.L., Broner, J., Deficiency of a glucocorticoid inducible isoenzyme of liver tyrosine aminotransferase in the obese C57BL-6J-ob mutant mouse. Biochem. Biophys. Res. Commun. 41 (1970), 1443–1451.
9. Dekker, J., Rippe, K., Dekker, M., Kleckner, N., Capturing chromosome conformation. Science 295 (2002), 1306–1311.
10. Do, R., Bailey, S.D., Paré, G., Montpetit, A., Desbiens, K., Hudson, T.J., Yusuf, S., Bouchard, C., Gaudet, D., Pérusse, L., et al. Fine mapping of the insulin-induced gene 2 identifies a variant associated with LDL cholesterol and total apolipoprotein B levels. Circ Cardiovasc Genet 3 (2010), 454–461.
11. Falandry, C., Fourel, G., Galy, V., Ristriani, T., Horard, B., Bensimon, E., Salles, G., Gilson, E., Magdinier, F., CLLD8/KMT1F is a lysine methyltransferase that is important for chromosome segregation. J. Biol. Chem. 285 (2010), 20234–20241.
12. Glaser, S., Schaft, J., Lubitz, S., Vintersten, K., van der Hoeven, F., Tufteland, K.R., Aasland, R., Anastassiadis, K., Ang, S.L., Stewart, A.F., Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133 (2006), 1423–1432.
13. Goldstein, I., Hager, G.L., Transcriptional and chromatin regulation during fasting—the genomic era. Trends Endocrinol. Metab. 26 (2015), 699–710.
14. Grøntved, L., John, S., Baek, S., Liu, Y., Buckley, J.R., Vinson, C., Aguilera, G., Hager, G.L., C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. EMBO J. 32 (2013), 1568–1583.
15. Haas, J.T., Miao, J., Chanda, D., Wang, Y., Zhao, E., Haas, M.E., Hirschey, M., Vaitheesvaran, B., Farese, R.V. Jr., Kurland, I.J., et al. Hepatic insulin signaling is required for obesity-dependent expression of SREBP-1c mRNA but not for feeding-dependent expression. Cell Metab. 15 (2012), 873–884.
16. Hagège, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W., Forné, T., Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc. 2 (2007), 1722–1733.
17. Hah, N., Murakami, S., Nagari, A., Danko, C.G., Kraus, W.L., Enhancer transcripts mark active estrogen receptor binding sites. Genome Res. 23 (2013), 1210–1223.
18. Hakim, O., John, S., Ling, J.Q., Biddie, S.C., Hoffman, A.R., Hager, G.L., Glucocorticoid receptor activation of the Ciz1-Lcn2 locus by long range interactions. J. Biol. Chem. 284 (2009), 6048–6052.
19. Herbert, A., Gerry, N.P., McQueen, M.B., Heid, I.M., Pfeufer, A., Illig, T., Wichmann, H.E., Meitinger, T., Hunter, D., Hu, F.B., et al. A common genetic variant is associated with adult and childhood obesity. Science 312 (2006), 279–283.
20. Horton, J.D.B., Bashmakov, Y., Shimomura, I., Shimano, H., Regulation of sterol regulatory element binding proteins in livers of fasted and refed mice. Proc. Natl. Acad. Sci. USA 95 (1998), 5987–5992.
21. Hotta, K., Nakamura, M., Nakata, Y., Matsuo, T., Kamohara, S., Kotani, K., Komatsu, R., Itoh, N., Mineo, I., Wada, J., et al. INSIG2 gene rs7566605 polymorphism is associated with severe obesity in Japanese. J. Hum. Genet. 53 (2008), 857–862.
22. Jeon, T.I., Osborne, T.F., SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol. Metab. 23 (2012), 65–72.
23. Kadmiel, M., Cidlowski, J.A., Glucocorticoid receptor signaling in health and disease. Trends Pharmacol. Sci. 34 (2013), 518–530.
24. Kaulfers, A.M., Deka, R., Dolan, L., Martin, L.J., Association of INSIG2 polymorphism with overweight and LDL in children. PLoS ONE, 10, 2015, e0116340.
25. Kotelevtsev, Y., Holmes, M.C., Burchell, A., Houston, P.M., Schmoll, D., Jamieson, P., Best, R., Brown, R., Edwards, C.R., Seckl, J.R., Mullins, J.J., 11beta-hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc. Natl. Acad. Sci. USA 94 (1997), 14924–14929.
26. Kroetz, D.N., Allen, R.M., Schaller, M.A., Cavallaro, C., Ito, T., Kunkel, S.L., Type I interferon induced epigenetic regulation of macrophages suppresses innate and adaptive immunity in acute respiratory viral infection. PLoS Pathog., 11, 2015, e1005338.
27. Lee, J., Saha, P.K., Yang, Q.H., Lee, S., Park, J.Y., Suh, Y., Lee, S.K., Chan, L., Roeder, R.G., Lee, J.W., Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc. Natl. Acad. Sci. USA 105 (2008), 19229–19234.
28. Lee, S., Lee, J., Lee, S.K., Lee, J.W., Activating signal cointegrator-2 is an essential adaptor to recruit histone H3 lysine 4 methyltransferases MLL3 and MLL4 to the liver X receptors. Mol. Endocrinol. 22 (2008), 1312–1319.
29. Lemke, U., Krones-Herzig, A., Berriel Diaz, M., Narvekar, P., Ziegler, A., Vegiopoulos, A., Cato, A.C., Bohl, S., Klingmüller, U., Screaton, R.A., et al. The glucocorticoid receptor controls hepatic dyslipidemia through Hes1. Cell Metab. 8 (2008), 212–223.
30. Liu, Y., Nakagawa, Y., Wang, Y., Li, R., Li, X., Ohzeki, T., Friedman, T.C., Leptin activation of corticosterone production in hepatocytes may contribute to the reversal of obesity and hyperglycemia in leptin-deficient ob/ob mice. Diabetes 52 (2003), 1409–1416.
31. Mishiro, T., Ishihara, K., Hino, S., Tsutsumi, S., Aburatani, H., Shirahige, K., Kinoshita, Y., Nakao, M., Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 28 (2009), 1234–1245.
32. Morton, N.M., Holmes, M.C., Fiévet, C., Staels, B., Tailleux, A., Mullins, J.J., Seckl, J.R., Improved lipid and lipoprotein profile, hepatic insulin sensitivity, and glucose tolerance in 11beta-hydroxysteroid dehydrogenase type 1 null mice. J. Biol. Chem. 276 (2001), 41293–41300.
33. Mozzetta, C., Boyarchuk, E., Pontis, J., Ait-Si-Ali, S., Sound of silence: the properties and functions of repressive Lys methyltransferases. Nat. Rev. Mol. Cell Biol. 16 (2015), 499–513.
34. Quax, R.A., Manenschijn, L., Koper, J.W., Hazes, J.M., Lamberts, S.W., van Rossum, E.F., Feelders, R.A., Glucocorticoid sensitivity in health and disease. Nat. Rev. Endocrinol. 9 (2013), 670–686.
35. Radhakrishnan, A., Ikeda, Y., Kwon, H.J., Brown, M.S., Goldstein, J.L., Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: oxysterols block transport by binding to Insig. Proc. Natl. Acad. Sci. USA 104 (2007), 6511–6518.
36. Rose, A.J., Vegiopoulos, A., Herzig, S., Role of glucocorticoids and the glucocorticoid receptor in metabolism: insights from genetic manipulations. J. Steroid Biochem. Mol. Biol. 122 (2010), 10–20.
37. Schliehe, C., Flynn, E.K., Vilagos, B., Richson, U., Swaminathan, S., Bosnjak, B., Bauer, L., Kandasamy, R.K., Griesshammer, I.M., Kosack, L., et al. The methyltransferase Setdb2 mediates virus-induced susceptibility to bacterial superinfection. Nat. Immunol. 16 (2015), 67–74.
38. Shimomura, I., Bashmakov, Y., Horton, J.D., Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J. Biol. Chem. 274 (1999), 30028–30032.
39. Shin, D.J., Joshi, P., Hong, S.H., Mosure, K., Shin, D.G., Osborne, T.F., Genome-wide analysis of FoxO1 binding in hepatic chromatin: potential involvement of FoxO1 in linking retinoid signaling to hepatic gluconeogenesis. Nucleic Acids Res. 40 (2012), 11499–11509.
40. Teperino, R., Schoonjans, K., Auwerx, J., Histone methyl transferases and demethylases; can they link metabolism and transcription?. Cell Metab. 12 (2010), 321–327.
41. Tsai, W.W.N., Niessen, S., Goebel, N., Yates, J.R. 3rd, Guccione, E., Montminy, M., PRMT5 modulates the metabolic response to fasting signals. Proc. Natl. Acad. Sci. USA 110 (2013), 8870–8875.
42. Völkel, P., Angrand, P.O., The control of histone lysine methylation in epigenetic regulation. Biochimie 89 (2007), 1–20.
43. Wong, S., Tan, K., Carey, K.T., Fukushima, A., Tiganis, T., Cole, T.J., Glucocorticoids stimulate hepatic and renal catecholamine inactivation by direct rapid induction of the dopamine sulfotransferase Sult1d1. Endocrinology 151 (2010), 185–194.
44. Yabe, D., Komuro, R., Liang, G., Goldstein, J.L., Brown, M.S., Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc. Natl. Acad. Sci. USA 100 (2003), 3155–3160.
45. Yahagi, N., Shimano, H., Hasty, A.H., Matsuzaka, T., Ide, T., Yoshikawa, T., Amemiya-Kudo, M., Tomita, S., Okazaki, H., Tamura, Y., et al. Absence of sterol regulatory element-binding protein-1 (SREBP-1) ameliorates fatty livers but not obesity or insulin resistance in Lep(ob)/Lep(ob) mice. J. Biol. Chem. 277 (2002), 19353–19357.
46. Zhang, F., Xu, X., Zhou, B., He, Z., Zhai, Q., Gene expression profile change and associated physiological and pathological effects in mouse liver induced by fasting and refeeding. PLoS ONE, 6, 2011, e27553.
47. Zhang, X., Peng, D., Xi, Y., Yuan, C., Sagum, C.A., Klein, B.J., Tanaka, K., Wen, H., Kutateladze, T.G., Li, W., et al. G9a-mediated methylation of ERα links the PHF20/MOF histone acetyltransferase complex to hormonal gene expression. Nat. Commun., 7, 2016, 10810.