Advertisement

Epigenetic Aspects of Nuclear Receptor Coregulators: How Nutritional and Environmental Signals Change Gene Expression Patterns

  • Fawaz AlzaïdEmail author
  • Tomas Jakobsson
  • Eckardt Treuter
  • Nicolas Venteclef
Reference work entry

Abstract

Nuclear receptor coregulators are a large family of proteins that interact with nuclear receptors at promoters and enhancers to alter gene expression. Modifications induced by coregulators will either amplify or suppress the rate of transcription. Nuclear receptors themselves are transcription factors that are stimulated by hormonal, metabolic, and environmental stimuli; they are then directed to target gene promoters to initiate transcription. The nature of the nuclear receptor ligand is a large determinant of which coregulator complexes are recruited, either recruiting coactivators or corepressors. Agonists generally recruit coactivators that amplify transcription, whereas antagonists will generally recruit corepressors that will dampen transcription. Interestingly, bivalent or dual-function coregulators have recently come to light. Their effects appear to be dependent on cell-type, tissue-type, and/or developmental stage; much remains to be elucidated with regards to this class of coregulators.

Once formed, the coregulator complex exerts its effects through multiple mechanisms that are largely dependent on editing the epigenome. Enzymes are recruited into coregulator complexes that act on chromatin, DNA, and on other coregulator complex subunits. Histone acetylases, deacetylases, methyltransferases, and demethylases are some of the most important enzymes in the control of the target gene promoter context. Acetylation is generally associated with coactivator activity, while methylation acts in both activation and repression. Another mechanism implicates repositioning, eviction, or exchange of nucleosome components in an ATP-dependent manner. These and many other post-translational modifications also affect coregulators themselves, being subject to sumoylation, phosphorylation, as well as acetylation and methylation. The dynamic regulation of both coregulators and epigenomes allows rapid adaptation to the cellular and metabolic milieu.

A large number of coregulator complexes have been shown to be extremely important in nutrition and metabolism. Adipose tissue and the liver have been extensively studied and have proven to be the major tissues in which coregulators and their epigenetic functions contribute to metabolic and nutritional adaptation. Interestingly coregulators have also been demonstrated to tightly control cellular metabolism and the inflammatory response, two key processes in nutritional and metabolic disease. This chapter describes the mechanisms through which coregulators exert their functions, with a particular emphasis on the epigenome. We also describe pertinent examples from scientific literature that demonstrate the epigenetic aspects on nuclear receptor coregulators in nutrition and metabolism.

Keywords

Coregulators Corepressors Coactivators Nuclear receptors Nutrition Metabolism Transcription Epigenetics Histone modification Chromatin 

List of Abbreviations

AF2

Activator function 2

AP

Associated protein

BAT

Brown adipose tissue

C/EBPα

CCAAT/enhancer-binding protein C/EBPα

CBP

p300/CREB binding protein

CDK4

Cyclin-dependent kinase 4

CoREST

Repressor element-1 silencing transcription factor corepressor 1

CYP7A1

Cholesterol hydroxylase

CYP8B1

Sterol hydroxylase

DNA

Deoxyribonucleic acid

DNMT

DNA methyltransferases

EHMT

Histone methyltransferase

ER

Estrogen receptor (NR3A1/2)

eRNA

Enhancer-associated RNA

GLUT

Glucose transporter

GNAT

Gcn5-related N-acetyltransferase

GPS2

G-protein pathway suppressor2

HAT

Histone acetyltransferase

HDAC

Histone deacetylase

HIF1 α

Hypoxia-inducible factor 1α

ISWI

Imitation switch

LBD

Ligand binding domain

LRH1

Liver receptor homolog 1 (NR5A2)

LSD/KDM

Lysine demethylases

LXR

Liver X receptor (NR1H2/3)

MYST

MOZ-Ybf2-Sas3-Tip60

NCOA

Nuclear receptor coactivator

NCoR

Nuclear receptor corepressor

NR

Nuclear receptor

PCAF

p300/CBP-associated factor

PGC1α

PPARγ coactivator

PROX1

Prospero homeobox protein 1

PTM

Post-translational modification

RAR

Retinoic acid receptor (NR1B1/2/3)

RIP140

Receptor-interacting protein 140

RNA

Ribonucleic acid

RNF4

RING finger protein 4

SAM

S-Adenosyl methionine

SET

Su (var) 3-9, enhancer of zeste, trithorax

SIRT

Sirtuin

SRA

Steroid receptor RNA activator

SUMO

Small ubiquitin-like modifiers

SWI/SNF

Switch/sucrose non-fermenting

TLE3

Transducin-like enhancer 3

TR

Thyroid hormone receptor (NR1A1/2)

TRIM24

Tripartite motif containing 24

UCP1

Uncoupling protein 1

WAT

White adipose tissue

References

  1. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, Christensen J, Helin K (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23(10):1171–1176CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baas T (2013) Closer to class IIa HDAC inhibitors. SciBX 6(13). Published Online:  https://doi.org/10.1038/scibx.2013.301
  3. Becnel LB, Darlington YF, Ochsner SA, Easton-Marks JR, Watkins CM, McOwiti A, Kankanamge WH, Wise MW, DeHart M, Margolis RN, McKenna NJ (2015) Nuclear receptor signaling atlas: opening access to the biology of nuclear receptor signaling pathways. PLoS One 10(9):e0135615CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bedford DC, Kasper LH, Wang R, Chang Y, Green DR, Brindle PK (2011) Disrupting the CH1 domain structure in the acetyltransferases CBP and p300 results in lean mice with increased metabolic control. Cell Metab 14(2):219–230CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A et al (2006) A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells. Cell 125 (2):315–326Google Scholar
  6. Cardamone MD, Tanasa B, Chan M, Cederquist CT, Andricovich J, Rosenfeld MG, Perissi V (2014) GPS2/KDM4A pioneering activity regulates promoter-specific recruitment of PPARgamma. Cell Rep 8(1):163–176CrossRefPubMedPubMedCentralGoogle Scholar
  7. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V, Fuller-Pace FV, Hoffman EP, Tapscott SJ, Sartorelli V (2006) The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 11(4):547–560CrossRefPubMedGoogle Scholar
  8. Chauchereau A, Amazit L, Quesne M, Guiochon-Mantel A, Milgrom E (2003) Sumoylation of the progesterone receptor and of the steroid receptor coactivator SRC-1. J Biol Chem 278(14):12335–12343CrossRefPubMedGoogle Scholar
  9. Chevillard-Briet M, Trouche D, Vandel L (2002) Control of CBP co-activating activity by arginine methylation. EMBO J 21(20):5457–5466CrossRefPubMedPubMedCentralGoogle Scholar
  10. Choi HK, Yoo JY, Jeong MH, Park SY, Shin DM, Jang SW, Yoon HG, Choi KC (2013) Protein kinase A phosphorylates NCoR to enhance its nuclear translocation and repressive function in human prostate cancer cells. J Cell Physiol 228(6):1159–1165CrossRefPubMedGoogle Scholar
  11. Coste A, Louet JF, Lagouge M, Lerin C, Antal MC, Meziane H, Schoonjans K, Puigserver P, O'Malley BW, Auwerx J (2008) The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1{alpha}. Proc Natl Acad Sci U S A 105(44):17187–17192CrossRefPubMedPubMedCentralGoogle Scholar
  12. Creixell P, Linding R (2012) Cells, shared memory and breaking the PTM code. Mol Syst Biol 8:598CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dasgupta S, O’Malley BW (2014) Transcriptional coregulators: emerging roles of SRC family of coactivators in disease pathology. J Mol Endocrinol 53(2):R47–R59CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dennis AP, Lonard DM, Nawaz Z, O'Malley BW (2005) Inhibition of the 26S proteasome blocks progesterone receptor-dependent transcription through failed recruitment of RNA polymerase II. J Steroid Biochem Mol Biol 94(4):337–346CrossRefPubMedGoogle Scholar
  15. Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6(8):227CrossRefPubMedPubMedCentralGoogle Scholar
  16. Drori S, Girnun GD, Tou L, Szwaya JD, Mueller E, Xia K, Shivdasani RA, Spiegelman BM (2005) Hic-5 regulates an epithelial program mediated by PPARgamma. Genes Dev 19(3):362–375CrossRefPubMedPubMedCentralGoogle Scholar
  17. Elder D (1984) Theory of epigenetic coding. J Theor Biol 108(3):327–332CrossRefPubMedGoogle Scholar
  18. Fan R, Toubal A, Goni S, Drareni K, Huang Z, Alzaid F, Ballaire R, Ancel P, Liang N, Damdimopoulos A, Hainault I, Soprani A, Aron-Wisnewsky J, Foufelle F, Lawrence T, Gautier JF, Venteclef N, Treuter E (2016) Loss of the co-repressor GPS2 sensitizes macrophage activation upon metabolic stress induced by obesity and type 2 diabetes. Nat Med 22(7):780–791CrossRefPubMedGoogle Scholar
  19. Fang S, Suh JM, Atkins AR, Hong SH, Leblanc M, Nofsinger RR, Yu RT, Downes M, Evans RM (2011) Corepressor SMRT promotes oxidative phosphorylation in adipose tissue and protects against diet-induced obesity and insulin resistance. Proc Natl Acad Sci U S A 108(8):3412–3417CrossRefPubMedPubMedCentralGoogle Scholar
  20. Fernandez-Majada V, Aguilera C, Villanueva A, Vilardell F, Robert-Moreno A, Aytes A, Real FX, Capella G, Mayo MW, Espinosa L, Bigas A (2007) Nuclear IKK activity leads to dysregulated notch-dependent gene expression in colorectal cancer. Proc Natl Acad Sci U S A 104(1):276–281CrossRefPubMedGoogle Scholar
  21. Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W, Verdin E (2002) Enzymatic activity associated with class II HDACs Is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Molecular Cell 9(1):45–57Google Scholar
  22. Foulds CE, Feng Q, Ding C, Bailey S, Hunsaker TL, Malovannaya A, Hamilton RA, Gates LA, Zhang Z, Li C, Chan D, Bajaj A, Callaway CG, Edwards DP, Lonard DM, Tsai SY, Tsai MJ, Qin J, O'Malley BW (2013) Proteomic analysis of coregulators bound to ERalpha on DNA and nucleosomes reveals coregulator dynamics. Mol Cell 51(2):185–199CrossRefPubMedPubMedCentralGoogle Scholar
  23. Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, Snowden AW, Garcia-Wilson E, Perkins ND, Hay RT (2003) P300 transcriptional repression is mediated by SUMO modification. Mol Cell 11(4):1043–1054CrossRefPubMedGoogle Scholar
  24. Glass CK, Saijo K (2010) Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nat Rev Immunol 10(5):365–376CrossRefPubMedGoogle Scholar
  25. Guenther MG, Barak O, Lazar MA (2001) The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Molecular and Cellular Biology 21(18):6091–6101Google Scholar
  26. Guidici M, Goni S, Fan R, Treuter E (2015) Nuclear receptor coregulators in metabolism and disease. Handbook of experimental pharmacology. PMID:25903414. Berlin, New York, Springer-Verlag.Google Scholar
  27. Gupta P, Huq MD, Khan SA, Tsai NP, Wei LN (2005) Regulation of co-repressive activity of and HDAC recruitment to RIP140 by site-specific phosphorylation. Mol Cell Proteomics 4(11):1776–1784CrossRefPubMedGoogle Scholar
  28. Hakli M, Lorick KL, Weissman AM, Janne OA, Palvimo JJ (2004) Transcriptional coregulator SNURF (RNF4) possesses ubiquitin E3 ligase activity. FEBS Lett 560(1–3):56–62CrossRefPubMedGoogle Scholar
  29. Halachmi S, Marden E, Martin G, MacKay H, Abbondanza C, Brown M (1994) Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science 264(5164):1455–1458CrossRefPubMedGoogle Scholar
  30. Harms MJ, Ishibashi J, Wang W, Lim HW, Goyama S, Sato T, Kurokawa M, Won KJ, Seale P (2014) Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metab 19(4):593–604CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hashizume R, Andor N, Ihara Y, Lerner R, Gan H, Chen X, Fang D, Huang X, Tom MW, Ngo V, Solomon D, Mueller S, Paris PL, Zhang Z, Petritsch C, Gupta N, Waldman TA, James CD (2014) Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med 20(12):1394–1396CrossRefPubMedPubMedCentralGoogle Scholar
  32. Haumaitre C, Lenoir O, Scharfmann R (2008) Histone deacetylase inhibitors modify pancreatic cell fate determination and amplify endocrine progenitors. Mol Cell Biol 28(20):6373–6383CrossRefPubMedPubMedCentralGoogle Scholar
  33. Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK et al (1995) Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377(6548):397–404CrossRefPubMedGoogle Scholar
  34. Huang N, vom Baur E, Garnier JM, Lerouge T, Vonesch JL, Lutz Y, Chambon P, Losson R (1998) Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators. EMBO J 17(12):3398–3412CrossRefPubMedPubMedCentralGoogle Scholar
  35. Huang P, Chandra V, Rastinejad F (2010) Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu Rev Physiol 72:247–272CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jakobsson T, Venteclef N, Toresson G, Damdimopoulos AE, Ehrlund A, Lou X, Sanyal S, Steffensen KR, Gustafsson JA, Treuter E (2009) GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol Cell 34(4):510–518CrossRefPubMedGoogle Scholar
  37. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293(5532):1074–1080CrossRefGoogle Scholar
  38. Jiang S, Minter LC, Stratton SA, Yang P, Abbas HA, Akdemir ZC, Pant V, Post S, Gagea M, Lee RG, Lozano G, Barton MC (2015) TRIM24 suppresses development of spontaneous hepatic lipid accumulation and hepatocellular carcinoma in mice. J Hepatol 62(2):371–379CrossRefPubMedGoogle Scholar
  39. Jonas BA, Privalsky ML (2004) SMRT and N-CoR corepressors are regulated by distinct kinase signaling pathways. J Biol Chem 279(52):54676–54686CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kemper JK, Xiao Z, Ponugoti B, Miao J, Fang S, Kanamaluru D, Tsang S, Wu SY, Chiang CM, Veenstra TD (2009) FXR acetylation is normally dynamically regulated by p300 and SIRT1 but constitutively elevated in metabolic disease states. Cell Metab 10(5):392–404CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kim HS, Xiao C, Wang RH, Lahusen T, Xu X, Vassilopoulos A, Vazquez-Ortiz G, Jeong WI, Park O, Ki SH, Gao B, Deng CX (2010) Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell Metab 12(3):224–236CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kim DH, Xiao Z, Kwon S, Sun X, Ryerson D, Tkac D, Ma P, Wu SY, Chiang CM, Zhou E, Xu HE, Palvimo JJ, Chen LF, Kemper B, Kemper JK (2015) A dysregulated acetyl/SUMO switch of FXR promotes hepatic inflammation in obesity. EMBO J 34(2):184–199CrossRefPubMedGoogle Scholar
  43. Kingston RE, Narlikar GJ (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13(18):2339–2352CrossRefPubMedGoogle Scholar
  44. Kiskinis E, Chatzeli L, Curry E, Kaforou M, Frontini A, Cinti S, Montana G, Parker MG, Christian M (2014) RIP140 represses the “brown-in-white” adipocyte program including a futile cycle of triacylglycerol breakdown and synthesis. Mol Endocrinol 28(3):344–356CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kugel JF, Goodrich JA (2012) Non-coding RNAs: key regulators of mammalian transcription. Trends Biochem Sci 37(4):144–151CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lee BH, Stallcup MR (2017) Glucocorticoid receptor binding to chromatin is selectively controlled by the coregulator Hic-5 and chromatin remodeling enzymes. J Biol Chem 292(22):9320–9334CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lee KK, Workman JL (2007) Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 8(4):284–295CrossRefPubMedGoogle Scholar
  48. Lee Y, Dominy JE, Choi YJ, Jurczak M, Tolliday N, Camporez JP, Chim H, Lim JH, Ruan HB, Yang X, Vazquez F, Sicinski P, Shulman GI, Puigserver P (2014) Cyclin D1-Cdk4 controls glucose metabolism independently of cell cycle progression. Nature 510(7506):547–551CrossRefPubMedPubMedCentralGoogle Scholar
  49. Leonardsson G, Steel JH, Christian M, Pocock V, Milligan S, Bell J, So PW, Medina-Gomez G, Vidal-Puig A, White R, Parker MG (2004) Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc Natl Acad Sci U S A 101(22):8437–8442CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lerin C, Rodgers JT, Kalume DE, Kim SH, Pandey A, Puigserver P (2006) GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha. Cell Metab 3(6):429–438CrossRefPubMedGoogle Scholar
  51. Leuenberger N, Pradervand S, Wahli W (2009) Sumoylated PPARalpha mediates sex-specific gene repression and protects the liver from estrogen-induced toxicity in mice. J Clin Invest 119(10):3138–3148CrossRefPubMedPubMedCentralGoogle Scholar
  52. Li P, Fan W, Xu J, Lu M, Yamamoto H, Auwerx J, Sears DD, Talukdar S, Oh D, Chen A, Bandyopadhyay G, Scadeng M, Ofrecio JM, Nalbandian S, Olefsky JM (2011) Adipocyte NCoR knockout decreases PPARgamma phosphorylation and enhances PPARgamma activity and insulin sensitivity. Cell 147(4):815–826CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li P, Spann NJ, Kaikkonen MU, Lu M, Oh DY, Fox JN, Bandyopadhyay G, Talukdar S, Xu J, Lagakos WS, Patsouris D, Armando A, Quehenberger O, Dennis EA, Watkins SM, Auwerx J, Glass CK, Olefsky JM (2013) NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids. Cell 155(1):200–214CrossRefPubMedPubMedCentralGoogle Scholar
  54. Liu TF, Vachharajani VT, Yoza BK, McCall CE (2012) NAD+−dependent sirtuin 1 and 6 proteins coordinate a switch from glucose to fatty acid oxidation during the acute inflammatory response. J Biol Chem 287(31):25758–25769CrossRefPubMedPubMedCentralGoogle Scholar
  55. Liu X, Huang Y, Yang D, Li X, Liang J, Lin L, Zhang M, Zhong K, Liang B, Li J (2014) Overexpression of TRIM24 is associated with the onset and progress of human hepatocellular carcinoma. PLoS One 9(1):e85462CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lonard DM, Nawaz Z, Smith CL, O’Malley BW (2000) The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol Cell 5(6):939–948CrossRefPubMedGoogle Scholar
  57. Louet JF, Chopra AR, Sagen JV, An J, York B, Tannour-Louet M, Saha PK, Stevens RD, Wenner BR, Ilkayeva OR, Bain JR, Zhou S, DeMayo F, Xu J, Newgard CB, O’Malley BW (2010) The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab 12(6):606–618CrossRefPubMedPubMedCentralGoogle Scholar
  58. Martin M, Kettmann R, Dequiedt F (2007) Class IIa histone deacetylases: regulating the regulators. Oncogene 26(37):5450–5467CrossRefPubMedGoogle Scholar
  59. McKenna B, Guo M, Reynolds A, Hara M, Stein R (2015) Dynamic recruitment of functionally distinct Swi/Snf chromatin remodeling complexes modulates Pdx1 activity in islet beta cells. Cell Rep 10(12):2032–2042CrossRefPubMedPubMedCentralGoogle Scholar
  60. Millard CJ, Watson PJ, Fairall L, Schwabe JW (2013) An evolving understanding of nuclear receptor coregulator proteins. J Mol Endocrinol 51(3):T23–T36CrossRefPubMedPubMedCentralGoogle Scholar
  61. Min J, Feng Q, Li Z, Zhang Y, Xu RM (2003) Structure of the catalytic domain of human DOT1L, a non-SET domain nucleosomal histone methyltransferase. Cell 112(5):711–723CrossRefPubMedGoogle Scholar
  62. Nagai Y, Yonemitsu S, Erion DM, Iwasaki T, Stark R, Weismann D, Dong J, Zhang D, Jurczak MJ, Loffler MG, Cresswell J, Yu XX, Murray SF, Bhanot S, Monia BP, Bogan JS, Samuel V, Shulman GI (2009) The role of peroxisome proliferator-activated receptor gamma coactivator-1 beta in the pathogenesis of fructose-induced insulin resistance. Cell Metab 9(3):252–264CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pedersen MT, Helin K (2010) Histone demethylases in development and disease. Trends Cell Biol 20(11):662–671CrossRefPubMedGoogle Scholar
  64. Ponugoti B, Kim DH, Xiao Z, Smith Z, Miao J, Zang M, Wu SY, Chiang CM, Veenstra TD, Kemper JK (2010) SIRT1 deacetylates and inhibits SREBP-1C activity in regulation of hepatic lipid metabolism. J Biol Chem 285(44):33959–33970CrossRefPubMedPubMedCentralGoogle Scholar
  65. Powelka AM, Seth A, Virbasius JV, Kiskinis E, Nicoloro SM, Guilherme A, Tang X, Straubhaar J, Cherniack AD, Parker MG, Czech MP (2006) Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes. J Clin Invest 116(1):125–136CrossRefPubMedGoogle Scholar
  66. Purushotham A, Xu Q, Lu J, Foley JF, Yan X, Kim DH, Kemper JK, Li X (2012) Hepatic deletion of SIRT1 decreases hepatocyte nuclear factor 1alpha/farnesoid X receptor signaling and induces formation of cholesterol gallstones in mice. Mol Cell Biol 32(7):1226–1236CrossRefPubMedPubMedCentralGoogle Scholar
  67. Qiang L, Lin HV, Kim-Muller JY, Welch CL, Gu W, Accili D (2011) Proatherogenic abnormalities of lipid metabolism in SirT1 transgenic mice are mediated through Creb deacetylation. Cell Metab 14(6):758–767CrossRefPubMedPubMedCentralGoogle Scholar
  68. Qiang L, Wang L, Kon N, Zhao W, Lee S, Zhang Y, Rosenbaum M, Zhao Y, Gu W, Farmer SR, Accili D (2012) Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Ppargamma. Cell 150(3):620–632CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ramirez J, Dege C, Kutateladze TG, Hagman J (2012) MBD2 and multiple domains of CHD4 are required for transcriptional repression by Mi-2/NuRD complexes. Mol Cell Biol 32(24):5078–5088CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434(7029):113–118CrossRefPubMedGoogle Scholar
  71. Rohm M, Sommerfeld A, Strzoda D, Jones A, Sijmonsma TP, Rudofsky G, Wolfrum C, Sticht C, Gretz N, Zeyda M, Leitner L, Nawroth PP, Stulnig TM, Berriel Diaz M, Vegiopoulos A, Herzig S (2013) Transcriptional cofactor TBLR1 controls lipid mobilization in white adipose tissue. Cell Metab 17(4):575–585CrossRefPubMedGoogle Scholar
  72. Sampley ML, Ozcan S (2012) Regulation of insulin gene transcription by multiple histone acetyltransferases. DNA Cell Biol 31(1):8–14CrossRefPubMedPubMedCentralGoogle Scholar
  73. Sanyal S, Bavner A, Haroniti A, Nilsson LM, Lundasen T, Rehnmark S, Witt MR, Einarsson C, Talianidis I, Gustafsson JA, Treuter E (2007) Involvement of corepressor complex subunit GPS2 in transcriptional pathways governing human bile acid biosynthesis. Proc Natl Acad Sci U S A 104(40):15665–15670CrossRefPubMedPubMedCentralGoogle Scholar
  74. Sareddy GR, Nair BC, Krishnan SK, Gonugunta VK, Zhang QG, Suzuki T, Miyata N, Brenner AJ, Brann DW, Vadlamudi RK (2013) KDM1 is a novel therapeutic target for the treatment of gliomas. Oncotarget 4(1):18–28CrossRefPubMedGoogle Scholar
  75. Sheppard HM, Harries JC, Hussain S, Bevan C, Heery DM (2001) Analysis of the steroid receptor coactivator 1 (SRC1)-CREB binding protein interaction interface and its importance for the function of SRC1. Mol Cell Biol 21(1):39–50CrossRefPubMedPubMedCentralGoogle Scholar
  76. Shiau AK, Barstad D, Loria PM, Cheng L, Kushner PJ, Agard DA, Greene GL (1998) The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95(7):927–937CrossRefPubMedGoogle Scholar
  77. Stein S, Oosterveer MH, Mataki C, Xu P, Lemos V, Havinga R, Dittner C, Ryu D, Menzies KJ, Wang X, Perino A, Houten SM, Melchior F, Schoonjans K (2014) SUMOylation-dependent LRH-1/PROX1 interaction promotes atherosclerosis by decreasing hepatic reverse cholesterol transport. Cell Metab 20(4):603–613CrossRefPubMedGoogle Scholar
  78. Sun G, Reddy MA, Yuan H, Lanting L, Kato M, Natarajan R (2010) Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 21(12):2069–2080CrossRefPubMedPubMedCentralGoogle Scholar
  79. Sun Z, Feng D, Fang B, Mullican SE, You SH, Lim HW, Everett LJ, Nabel CS, Li Y, Selvakumaran V, Won KJ, Lazar MA (2013) Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol Cell 52(6):769–782CrossRefPubMedGoogle Scholar
  80. Sun C, Wang M, Liu X, Luo L, Li K, Zhang S, Wang Y, Yang Y, Ding F, Gu X (2014) PCAF improves glucose homeostasis by suppressing the gluconeogenic activity of PGC-1alpha. Cell Rep 9(6):2250–2262CrossRefPubMedGoogle Scholar
  81. Teyssier C, Ma H, Emter R, Kralli A, Stallcup MR (2005) Activation of nuclear receptor coactivator PGC-1alpha by arginine methylation. Genes Dev 19(12):1466–1473CrossRefPubMedPubMedCentralGoogle Scholar
  82. Timinskas A, Butkus V, Janulaitis A (1995) Sequence motifs characteristic for DNA [cytosine-N4] and DNA [adenine-N6] methyltransferases. Classification of all DNA methyltransferases. Gene 157(1–2):3–11CrossRefPubMedGoogle Scholar
  83. Toubal A, Clement K, Fan R, Ancel P, Pelloux V, Rouault C, Veyrie N, Hartemann A, Treuter E, Venteclef N (2013) SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J Clin Invest 123(1):362–379CrossRefPubMedGoogle Scholar
  84. Treuter E, Venteclef N (2011) Transcriptional control of metabolic and inflammatory pathways by nuclear receptor SUMOylation. Biochim Biophys Acta 1812(8):909–918CrossRefPubMedGoogle Scholar
  85. Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, Ellis E, Nilsson LM, Parini P, Janne OA, Gustafsson JA, Steffensen KR, Treuter E (2010) GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev 24(4):381–395CrossRefPubMedPubMedCentralGoogle Scholar
  86. Villanueva CJ, Vergnes L, Wang J, Drew BG, Hong C, Tu Y, Hu Y, Peng X, Xu F, Saez E, Wroblewski K, Hevener AL, Reue K, Fong LG, Young SG, Tontonoz P (2013) Adipose subtype-selective recruitment of TLE3 or Prdm16 by PPARγ specifies lipid storage versus thermogenic gene programs. Cell Metab 17(3):423–435CrossRefPubMedPubMedCentralGoogle Scholar
  87. Vinogradova M, Gehling VS, Gustafson A, Arora S, Tindell CA, Wilson C, Williamson KE, Guler GD, Gangurde P, Manieri W, Busby J, Flynn EM, Lan F, Kim HJ, Odate S, Cochran AG, Liu Y, Wongchenko M, Yang Y, Cheung TK, Maile TM, Lau T, Costa M, Hegde GV, Jackson E, Pitti R, Arnott D, Bailey C, Bellon S, Cummings RT, Albrecht BK, Harmange JC, Kiefer JR, Trojer P, Classon M (2016) An inhibitor of KDM5 demethylases reduces survival of drug-tolerant cancer cells. Nat Chem Biol 12(7):531–538CrossRefPubMedGoogle Scholar
  88. Walsh CA, Bolger JC, Byrne C, Cocchiglia S, Hao Y, Fagan A, Qin L, Cahalin A, McCartan D, McIlroy M, O'Gaora P, Xu J, Hill AD, Young LS (2014) Global gene repression by the steroid receptor coactivator SRC-1 promotes oncogenesis. Cancer Res 74(9):2533–2544CrossRefPubMedGoogle Scholar
  89. Wang GG, Allis CD, Chi P (2007) Chromatin remodeling and cancer, part II: ATP-dependent chromatin remodeling. Trends Mol Med 13(9):373–380CrossRefPubMedPubMedCentralGoogle Scholar
  90. Wang C, Powell MJ, Popov VM, Pestell RG (2008) Acetylation in nuclear receptor signaling and the role of sirtuins. Mol Endocrinol 22(3):539–545CrossRefPubMedGoogle Scholar
  91. Warnmark A, Treuter E, Wright AP, Gustafsson JA (2003) Activation functions 1 and 2 of nuclear receptors: molecular strategies for transcriptional activation. Mol Endocrinol 17(10):1901–1909CrossRefPubMedGoogle Scholar
  92. Weems JC, Griesel BA, Olson AL (2012) Class II histone deacetylases downregulate GLUT4 transcription in response to increased cAMP signaling in cultured adipocytes and fasting mice. Diabetes 61(6):1404–1414CrossRefPubMedPubMedCentralGoogle Scholar
  93. Wu RC, Qin J, Hashimoto Y, Wong J, Xu J, Tsai SY, Tsai MJ, O’Malley BW (2002) Regulation of SRC-3 (pCIP/ACTR/AIB-1/RAC-3/TRAM-1) coactivator activity by I kappa B kinase. Mol Cell Biol 22(10):3549–3561CrossRefPubMedPubMedCentralGoogle Scholar
  94. Xiong Y, Wang E, Huang Y, Guo X, Yu Y, Du Q, Ding X, Sun Y (2016) Inhibition of lysine-specific Demethylase-1 (LSD1/KDM1A) promotes the adipogenic differentiation of hESCs through H3K4 methylation. Stem Cell Rev 12(3):298–304CrossRefPubMedPubMedCentralGoogle Scholar
  95. Xu Y, Zhang S, Lin S, Guo Y, Deng W, Zhang Y, Xue Y (2017) WERAM: a database of writers, erasers and readers of histone acetylation and methylation in eukaryotes. Nucleic Acids Res 45(D1):D264–D270PubMedGoogle Scholar
  96. Yuan H, Reddy MA, Sun G, Lanting L, Wang M, Kato M, Natarajan R (2013) Involvement of p300/CBP and epigenetic histone acetylation in TGF-beta1-mediated gene transcription in mesangial cells. Am J Physiol Renal Physiol 304(5):F601–F613CrossRefPubMedGoogle Scholar
  97. Zechner C, Lai L, Zechner JF, Geng T, Yan Z, Rumsey JW, Collia D, Chen Z, Wozniak DF, Leone TC, Kelly DP (2010) Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell Metab 12(6):633–642CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zhang X, Cheng X (2003) Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides. Structure 11(5):509–520CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zschiedrich I, Hardeland U, Krones-Herzig A, Berriel Diaz M, Vegiopoulos A, Muggenburg J, Sombroek D, Hofmann TG, Zawatzky R, Yu X, Gretz N, Christian M, White R, Parker MG, Herzig S (2008) Coactivator function of RIP140 for NFkappaB/RelA-dependent cytokine gene expression. Blood 112(2):264–276CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Fawaz Alzaïd
    • 1
    Email author
  • Tomas Jakobsson
    • 2
  • Eckardt Treuter
    • 3
  • Nicolas Venteclef
    • 1
  1. 1.Sorbonne Universités, Université Pierre et Marie-Curie, Institut National de la Santé et de la Recherche Médicale (INSERM), UMR_S 1138 Cordeliers ResearchParisFrance
  2. 2.Department of Laboratory MedicineKarolinska InstitutetHuddingeSweden
  3. 3.Department of Biosciences and NutritionKarolinska InstitutetHuddingeSweden

Personalised recommendations