ERRγ: a Junior Orphan with a Senior Role in Metabolism

Trends in Endocrinology and Metabolism

Volumn 28, Issue 4, 2017, Pages 261-272

  Misra, Jagannath ^a   Kim, Don Kyu ^a   Choi, Hueng Sik ^a  

^a Chonnam National University   (South Korea)

Author keywords

cell signaling; estrogen related receptor ; gene regulation; orphan nuclear receptor

Indexed keywords

ESTROGEN RECEPTOR; ESTROGEN RELATED RECEPTOR GAMMA; ORPHAN NUCLEAR RECEPTOR; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ESRRG PROTEIN, HUMAN;

ALCOHOL LIVER DISEASE; ALCOHOL METABOLISM; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENE TARGETING; GLUCOSE HOMEOSTASIS; HEART; HEART VENTRICLE HYPERTROPHY; HUMAN; INSULIN RESISTANCE; IRON METABOLISM; LIVER INJURY; METABOLIC DISORDER; METABOLISM; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SKELETAL MUSCLE; TRANSCRIPTION INITIATION; ANIMAL; GENETICS; LIVER; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; LIVER; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 85012931830     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2016.12.005     Document Type: Review

References (71)

1. 1 Giguere, V., Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 29 (2008), 677–696.
2. 2 Audet-Walsh, E., Giguere, V., The multiple universes of estrogen-related receptor alpha and gamma in metabolic control and related diseases. Acta Pharmacol Sin 36 (2015), 51–61.
3. 3 Huss, J.M., et al. Constitutive activities of estrogen-related receptors: Transcriptional regulation of metabolism by the ERR pathways in health and disease. Biochim Biophys Acta 1852 (2015), 1912–1927.
4. 4 Eudy, J.D., et al. Isolation of a gene encoding a novel member of the nuclear receptor superfamily from the critical region of usher syndrome type IIa at 1q41. Genomics 50 (1998), 382–384.
5. 5 Hong, H., et al. Hormone-independent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J Biol Chem 274 (1999), 22618–22626.
6. 6 Alaynick, W.A., et al. ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab 6 (2007), 13–24.
7. 7 Narkar, V.A., et al. Exercise and PGC-1alpha-independent synchronization of type I muscle metabolism and vasculature by ERRγ. Cell Metab 13 (2011), 283–293.
8. 8 Wang, T., et al. Estrogen-related receptor α (ERRα) and ERR ERRγ are essential coordinators of cardiac metabolism and function. Mol Cell Biol 35 (2015), 1281–1298.
9. 9 Alaynick, W.A., et al. ERRgamma regulates cardiac, gastric, and renal potassium homeostasis. Mol Endocrinol 24 (2010), 299–309.
10. 10 Gan, Z., et al. Nuclear receptor/microRNA circuitry links muscle fiber type to energy metabolism. J Clin Invest 123 (2013), 2564–2575.
11. 11 Luo, Y., et al. Estrogen-related receptor gamma (ERRgamma) regulates oxygen-dependent expression of voltage-gated potassium (K+) channels and tissue kallikrein during human trophoblast differentiation. Mol Endocrinol 27 (2013), 940–952.
12. 12 Kim, D.K., et al. Estrogen-related receptor gamma (ERRgamma) is a novel transcriptional regulator of phosphatidic acid phosphatase, LIPIN1, and inhibits hepatic insulin signaling. J Biol Chem 286 (2011), 38035–38042.
13. 13 Kim, D.K., et al. Orphan nuclear receptor estrogen-related receptor gamma (ERRgamma) is key regulator of hepatic gluconeogenesis. J Biol Chem 287 (2012), 21628–21639.
14. 14 Zhang, Y., et al. Orphan nuclear receptor oestrogen-related receptor gamma (ERRgamma) plays a key role in hepatic cannabinoid receptor type 1-mediated induction of CYP7A1 gene expression. Biochem J 470 (2015), 181–193.
15. 15 Jung, Y.S., et al. The orphan nuclear receptor ERRγ regulates hepatic CB1 receptor-mediated fibroblast growth factor 21 gene expression. PLoS One, 11, 2016, e0159425.
16. 16 Greschik, H., et al. Structural basis for the deactivation of the estrogen-related receptor gamma by diethylstilbestrol or 4-hydroxytamoxifen and determinants of selectivity. J Biol Chem 279 (2004), 33639–33646.
17. 17 Chao, E.Y., et al. Structure-guided synthesis of tamoxifen analogs with improved selectivity for the orphan ERRgamma. Bioorg Med Chem Lett 16 (2006), 821–824.
18. 18 Zuercher, W.J., et al. Identification and structure–activity relationship of phenolic acyl hydrazones as selective agonists for the estrogen-related orphan nuclear receptors ERRβ and ERRγ. J Med Chem 48 (2005), 3107–3109.
19. 19 Tohme, M., et al. Estrogen-related receptor gamma is an in vivo receptor of bisphenol A. Faseb J 28 (2014), 3124–3133.
20. 20 Greschik, H., et al. Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. Mol Cell 9 (2002), 303–313.
21. 21 Kim, D.K., et al. Inverse agonist of nuclear receptor ERRgamma mediates antidiabetic effect through inhibition of hepatic gluconeogenesis. Diabetes 62 (2013), 3093–3102.
22. 22 Misra, J., et al. O-GlcNAcylation of orphan nuclear receptor ERRgamma promotes hepatic gluconeogenesis. Diabetes 65 (2016), 2835–2848.
23. 23 Maccarrone, M., et al. Endocannabinoid signaling at the periphery: 50 years after THC. Trends in Pharmacological Sciences 36 (2015), 277–296.
24. 24 Kim, D.K., et al. Estrogen-related receptor gamma controls hepatic CB1 receptor-mediated CYP2E1 expression and oxidative liver injury by alcohol. Gut 62 (2013), 1044–1054.
25. 25 Kim, D.K., et al. Inverse agonist of estrogen-related receptor gamma controls Salmonella typhimurium infection by modulating host iron homeostasis. Nat Med 20 (2014), 419–424.
26. 26 Lee, J.H., et al. Hypoxia induces PDK4 gene expression through induction of the orphan nuclear receptor ERRγ. PLoS One, 7, 2012, e46324.
27. 27 Kumar, P., Mendelson, C.R., Estrogen-related receptor gamma (ERRgamma) mediates oxygen-dependent induction of aromatase (CYP19) gene expression during human trophoblast differentiation. Mol Endocrinol 25 (2011), 1513–1526.
28. 28 Misra, J., et al. Transcriptional cross talk between orphan nuclear receptor ERRgamma and transmembrane transcription factor ATF6α coordinates endoplasmic reticulum stress response. Nucleic Acids Res 41 (2013), 6960–6974.
29. 29 Kwon, D.H., et al. Estrogen-related receptor gamma induces cardiac hypertrophy by activating GATA4. J Mol Cell Cardiol 65 (2013), 88–97.
30. 30 Kida, Y.S., et al. ERRs Mediate a metabolic switch required for somatic cell reprogramming to pluripotency. Cell Stem Cell 16 (2015), 547–555.
31. 31 Yoshihara, E., et al. ERRgamma is required for the metabolic maturation of therapeutically functional glucose-responsive β cells. Cell Metab 23 (2016), 622–634.
32. 32 Gantner, M.L., et al. Complementary roles of estrogen-related receptors in brown adipocyte thermogenic function. Endocrinology 157 (2016), 4770–4781.
33. 33 Dixen, K., et al. ERRgamma enhances UCP1 expression and fatty acid oxidation in brown adipocytes. Obesity 21 (2013), 516–524.
34. 34 Gantne, M.L., et al. GADD45gamma regulates the thermogenic capacity of brown adipose tissue. Proc Natl Acad Sci U S A 111 (2014), 11870–11875.
35. 35 Rangwala, S.M., et al. Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285 (2010), 22619–22629.
36. 36 Badin, P.M., et al. Exercise-like effects by Estrogen-related receptor-gamma in muscle do not prevent insulin resistance in db/db mice. Sci Rep, 6, 2016, 26442.
37. 37 Devarakonda, S., et al. Disorder-to-order transition underlies the structural basis for the assembly of a transcriptionally active PGC-1α/ERRγ complex. Proc Natl Acad Sci U S A 108 (2011), 18678–18683.
38. 38 Takacs, M., et al. The asymmetric binding of PGC-1alpha to the ERRalpha and ERRgamma nuclear receptor homodimers involves a similar recognition mechanism. PLoS One, 8, 2013, e67810.
39. 39 Wang, L., et al. The orphan nuclear receptor SHP regulates PGC-1alpha expression and energy production in brown adipocytes. Cell Metab 2 (2005), 227–238.
40. 40 Sanyal, S., et al. Differential regulation of the orphan nuclear receptor small heterodimer partner gene promoter by orphan nuclear receptor ERR isoforms. J Biol Chem 277 (2002), 1739–1748.
41. 41 Park, Y.Y., et al. An autoregulatory loop controlling orphan nuclear receptor DAX-1 gene expression by orphan nuclear receptor ERRgamma. Nucleic Acids Res 33 (2005), 6756–6768.
42. 42 Xie, Y.B., et al. Transcriptional corepressor SMILE recruits SIRT1 to inhibit nuclear receptor estrogen receptor-related receptor gamma transactivation. J Biol Chem 284 (2009), 28762–28774.
43. 43 Nedumaran, B., et al. DAX-1 acts as a novel corepressor of orphan nuclear receptor HNF4alpha and negatively regulates gluconeogenic enzyme gene expression. J Biol Chem 284 (2009), 27511–27523.
44. 44 Lee, J.M., et al. Insulin-inducible SMILE inhibits hepatic gluconeogenesis. Diabetes 65 (2016), 62–73.
45. 45 Kim, D.K., et al. Orphan nuclear receptor SHP regulates iron metabolism through inhibition of BMP6-mediated hepcidin expression. Sci Rep, 6, 2016, 34630.
46. 46 Castet, A., et al. Receptor-interacting protein 140 differentially regulates estrogen receptor-related receptor transactivation depending on target genes. Mol Endocrinol 20 (2006), 1035–1047.
47. 47 Yasumoto, H., et al. GNL3L inhibits activity of estrogen-related receptor gamma by competing for coactivator binding. J Cell Sci 120 (2007), 2532–2543.
48. 48 Kim, D.K., et al. PKB/Akt phosphorylation of ERRgamma contributes to insulin-mediated inhibition of hepatic gluconeogenesis. Diabetologia 57 (2014), 2576–2585.
49. 49 Heckler, M.M., et al. ERK/MAPK regulates ERRγ expression, transcriptional activity and receptor-mediated tamoxifen resistance in ER+ breast cancer. FEBS J 281 (2014), 2431–2442.
50. 50 Tremblay, A.M., et al. Phosphorylation-dependent sumoylation regulates estrogen-related receptor-alpha. Mol Endocrinol 22 (2008), 570–584.
51. 51 Ren, Y., et al. Parkin degrades estrogen-related receptors to limit the expression of monoamine oxidases. Hum Mol Genet 20 (2011), 1074–1083.
52. 52 Kim, J.H., et al. Estrogen-related receptor gamma plays a key role in vascular calcificationthrough the upregulation of BMP2 expression. Arterioscler Thromb Vasc Biol 35 (2015), 2384–2390.
53. 53 Poidatz, D., et al. Trophoblast syncytialisation necessitates mitochondrial function through estrogen-related receptor-γ activation. Mol Hum Reprod 21 (2015), 206–216.
54. 54 Luo, Y., et al. Estrogen-related receptor gamma serves a role in blood pressure homeostasis during pregnancy. Mol Endocrinol 28 (2014), 965–975.
55. 55 Zhang, Y., et al. Estrogen-related receptors stimulate pyruvate dehydrogenase kinase isoform 4 gene expression. J Biol Chem 281 (2006), 39897–39906.
56. 56 Dufour, C.R., et al. Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and gamma. Cell Metab 5 (2007), 345–356.
57. 57 Han, Y.H., et al. RORalpha switches transcriptional mode of ERRgamma that results in transcriptional repression of CYP2E1 under ethanol-exposure. Nucleic Acids Res 44 (2016), 1095–1104.
58. 58 Saito, Y., et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9 (2006), 435–443.
59. 59 Song, G.S., Wang, L., Transcriptional mechanism for the paired miR-433 and miR-127 genes by nuclear receptors SHP and ERR gamma. Nucleic Acids Research 36 (2008), 5727–5735.
60. 60 Eichner, L.J., et al. miR-378(*) mediates metabolic shift in breast cancer cells via the PGC-1beta/ERRgamma transcriptional pathway. Cell Metab 12 (2010), 352–361.
61. 61 Misra, J., et al. Orphan nuclear receptor Errγ induces c-reactive protein gene expression through induction of er-bound bzip transmembrane transcription factor CREBH. Plos One, 9, 2015, e86342.
62. 62 Vecchi, C., et al. Gluconeogenic signals regulate iron homeostasis via hepcidin in mice. Gastroenterology 146 (2014), 1060–1069.
63. 63 Lasheras, J., et al. Gene expression profiling in hearts of diabetic mice uncovers a potential role of estrogen-related receptor γ in diabetic cardiomyopathy. Mol Cell Endocrinol 430 (2016), 77–88.
64. 64 Jeong, B.C., et al. The orphan nuclear receptor estrogen receptor-related receptor gamma negatively regulates BMP2-induced osteoblast differentiation and bone formation. J Biol Chem 284 (2009), 14211–14218.
65. 65 Cardelli, M., Aubin, J.E., ERRγ is not required for skeletal development but is a RUNX2-dependent negative regulator of postnatal bone formation in male mice. PLoS ONE, 9, 2014, e109592.
66. 66 Cho, Y., et al. Peroxisome proliferator-activated receptor gamma coactivator 1 (PGC-1)- and estrogen-related receptor (ERR)-induced regulator in muscle 1 (Perm1) is a tissue-specific regulator of oxidative capacity in skeletal muscle cells. J Biol Chem 288 (2013), 25207–25218.
67. 67 Murray, J., et al. Impaired myogenesis in estrogen-related receptor gamma (ERRgamma)-deficient skeletal myocytes due to oxidative stress. Faseb J 27 (2013), 135–150.
68. 68 Matsakas, A., et al. Revascularization of ischemic skeletal muscle by estrogen-related receptor-gamma. Circ Res 110 (2012), 1087–1096.
69. 69 Matsakas, A., et al. Muscle ERRgamma mitigates Duchenne muscular dystrophy via metabolic and angiogenic reprogramming. Faseb J 27 (2013), 4004–4016.
70. 70 Pei, L., et al. Dependence of hippocampal function on ERRgamma-regulated mitochondrial metabolism. Cell Metab 21 (2015), 628–636.
71. 71 Byerly, M.S., et al. Estrogen-related receptor beta deletion modulates whole-body energy balance via estrogen-related receptor γ and attenuates neuropeptide Y gene expression. Eur J Neurosci 37 (2013), 1033–1047.