The estrogen-related receptor alpha: the oldest, yet an energetic orphan with robust biological functions

References

• Evans RM. The steroid and thyroid hormone receptor superfamily. Science 1988, 240, 889–95.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM. The nuclear receptor superfamily: the second decade. Cell 1995, 83, 835–9.
   PubMed Web of Science ®Google Scholar
• Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ. Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 2006,126, 789–99.
   PubMed Web of Science ®Google Scholar
• Benoit G, Cooney A, Giguere V Ingraham H, Lazar M, Muscat G, Perlmann T, Renaud JP, Schwabe J, Sladek F, Tsai MJ, Laudet V. International Union of Pharmacology. LXVI. Orphan nuclear receptors. Pharmacol Rev 2006, 58, 798–836.
   PubMed Web of Science ®Google Scholar
• Hong H, Yang L, Stallcup MR. Hormone-independent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J Biol Chem 1999, 274, 22618–26.
   PubMed Web of Science ®Google Scholar
• Coward P, Lee D, Hull MV, Lehmann JM. 4-Hydroxytamoxifen binds to and deactivates the estrogen-related receptor α. Proc Natl Acad Sci U S A 2001, 98, 8880–4.
   PubMed Web of Science ®Google Scholar
• Giguere V, Yang N, Segui P, Evans RM. Identification of a new class of steroid hormone receptors. Nature 1988, 331, 91–4.
   PubMed Web of Science ®Google Scholar
• Giguere V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 2008, 29, 677–96.
   PubMed Web of Science ®Google Scholar
• Giguere V. To ERR in the estrogen pathway. Trends Endocrinol Metab 2002, 13, 220–5.
   PubMed Web of Science ®Google Scholar
• Johnston SD, Liu X, Zuo F, Eisenbraun TL, Wiley SR, Kraus RJ, Mertz JE. Estrogen-related receptor alpha 1 functionally binds as a monomer to extended half-site sequences including ones contained within estrogen-response elements. Mol Endocrinol 1997, 11, 342–52.
   PubMed Web of Science ®Google Scholar
• Yang N, Shigeta H, Shi H, Teng CT. Estrogen-related receptor, hERR1, modulates estrogen receptor-mediated response of human lactoferrin gene promoter. J Biol Chem 1996, 271, 5795–804.
   PubMed Web of Science ®Google Scholar
• Sonoda J, Laganière J, Mehl IR, Barish GD, Chong LW, Li X, Scheffler IE, Mock DC, Bataille AR, Robert F, Lee CH, Giguère V, Evans RM. Nuclear receptor ERRalpha and coactivator PGC-1beta are effectors of IFN-gamma-induced host defense. Genes Dev 2007, 21, 1909–20.
   PubMed Web of Science ®Google Scholar
• Ichida M, Nemoto S, Finkel T. Identification of a specific molecular repressor of the peroxisome proliferator-activated receptor gamma coactivator-1 alpha. J Biol Chem 2002, 277, 50991–5.
   PubMed Web of Science ®Google Scholar
• Dufour CR, Wilson BJ, Huss JM, Kelly DP, Alaynick WA, Downes M, Evans RM, Blanchette M, Giguère V. Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and gamma. Cell Metab 2007, 5, 345–56.
   PubMed Web of Science ®Google Scholar
• Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122, 33–43.
   PubMed Web of Science ®Google Scholar
• Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M. Genome-wide analysis of estrogen receptor binding sites. Nat Genet 2006, 38, 1289–97.
   PubMed Web of Science ®Google Scholar
• Mootha VK, Handschin C, Arlow D, Xie X, St Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, Willy PJ, Schulman IG, Heyman RA, Lander ES, Spiegelman BM. ERR alpha and Gabpa/b specify PGC-1 alpha dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci U S A 2004, 101, 6570–5.
   PubMed Web of Science ®Google Scholar
• Schreiber SN, Emter R, Hock MB, Knutti D, Cardenas J, Podvinec M, Oakeley EJ, Kralli A. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci U S A 2004, 101, 6472–7.
   PubMed Web of Science ®Google Scholar
• Gaillard S, Grasfeder LL, Haeffele CL, Lobenhofer EK, Chu TM, Wolfinger R, Kazmin D, Koves TR, Muoio DM, Chang CY, McDonnell DP. Receptor-selective coactivators as tools to define the biology of specific receptor–coactivator pairs. Mol Cell 2006, 24, 797–803.
   PubMed Web of Science ®Google Scholar
• Tremblay AM, Giguere V. The NR3B subgroup: an ovERRview. Nucl Recept Signal 2007, 5, e009.
   PubMedGoogle Scholar
• Luo J, Sladek R, Carrier J, Bader JA, Richard D, Giguère V. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol Cell Biol 2003, 23, 7947–56.
   PubMed Web of Science ®Google Scholar
• Huss JM, Torra IP, Staels B, Giguère V, Kelly DP. Estrogen-related receptor α directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol Cell Biol 2004, 24, 9079–91.
   PubMed Web of Science ®Google Scholar
• Carrier JC, Deblois G, Champigny C, Levy E, Giguère V. Estrogen-related receptor alpha (ERRalpha) is a transcriptional regulator of apolipoprotein A-IV and controls lipid handling in the intestine. J Biol Chem 2004, 279, 52052–8.
   PubMed Web of Science ®Google Scholar
• Cartoni R, Léger B, Hock MB, Praz M, Crettenand A, Pich S, Ziltener JL, Luthi F, Dériaz O, Zorzano A, Gobelet C, Kralli A, Russell AP. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J Physiol 2005, 567, 349–58.
   PubMed Web of Science ®Google Scholar
• Schreiber SN, Knutti D, Brogli K, Uhlmann T, Kralli A. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor alpha (ERRalpha). J Biol Chem 2003, 278, 9013–8.
   PubMed Web of Science ®Google Scholar
• Herzog B, Cardenas J, Hall RK, Villena JA, Budge PJ, Giguere V, Granner DK, Kralli A. Estrogen-related receptor alpha is a repressor of phosphoenolpyruvate carboxykinase gene transcription. J Biol Chem 2006, 281, 99–106.
   PubMed Web of Science ®Google Scholar
• Wende AR, Huss JM, Schaeffer PJ, Giguere V, Kelly DP. PGC-1 alpha coactivates PDK4 gene expression via the orphan nuclear receptor ERR alpha: a mechanism for transcriptional control of muscle glucose metabolism. Mol Cell Biol 2005, 25, 10684–94.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Ma K, Sadana P, Chowdhury F, Gaillard S, Wang F, McDonnell DP, Unterman TG, Elam MB, Park EA. Estrogen related receptors stimulate pyruvate dehydrogenase kinase isoform 4 gene expression. J Biol Chem 2006, 281, 39897–906.
   PubMed Web of Science ®Google Scholar
• Villena JA, Hock MB, Giguere V, Kralli A. Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc Natl Acad Sci U S A 2007, 104, 1418–23.
   PubMed Web of Science ®Google Scholar
• Nagao M, Parimoo B, Tanaka K. Developmental, nutritional, and hormonal regulation of tissue-specific expression of the genes encoding various acyl-CoA dehydrogenases and α-subunit of electron transfer flavoprotein in rat. J Biol Chem 1993, 268, 24114–24.
   PubMed Web of Science ®Google Scholar
• Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR, Stahl E, Bolouri MS, Ray HN, Sihag S, Kamal M, Patterson N, Lander ES, Mann M. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115, 629–40.
   PubMed Web of Science ®Google Scholar
• Soriano FX, Liesa M, Bach D, Chan DC, Palacin M, Zorzano A. Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-gamma coactivator-1 alpha, estrogen-related receptor alpha, and mitofusin 2. Diabetes 2006, 55, 1783–91.
   PubMed Web of Science ®Google Scholar
• Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev 2006, 86, 465–514.
   PubMed Web of Science ®Google Scholar
• Sladek R, Giguere V. Orphan nuclear receptors: an emerging family of metabolic regulators. Adv Pharmacol 2000, 47, 23–87.
   PubMedGoogle Scholar
• Hummasti S, Tontonoz P. Adopting new orphans into the family of metabolic regulators. Mol Endocrinol 2008, 22, 1743–53.
   PubMedGoogle Scholar
• Ranhotra HS. Up-regulation of orphan nuclear estrogen-related receptor alpha expression during long-term caloric restriction in mice. Mol Cell Biochem 2009, 332, 59–65.
   PubMed Web of Science ®Google Scholar
• Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004, 84, 277–359.
   PubMed Web of Science ®Google Scholar
• Castet A, Herledan A, Bonnet S, Jalaguier S, Vanacker JM, Cavailles V. Receptor-interacting protein 140 differentially regulates estrogen receptor-related receptor transactivation depending on target genes. Mol Endocrinol 2006, 20, 1035–47.
   PubMed Web of Science ®Google Scholar
• Nichol D, Christian M, Steel JH, White R, Parker MG. RIP140 expression is stimulated by estrogen-related receptor alpha during adipogenesis. J Biol Chem 2006, 281, 32140–7.
   PubMed Web of Science ®Google Scholar
• Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest 2005, 115, 547–55.
   PubMed Web of Science ®Google Scholar
• Lehman JJ, Kelly DP. Transcriptional activation of energy metabolic switches in the developing and hypertrophied heart. Clin Exp Pharmacol Physiol 2002, 29, 339–45.
   Google Scholar
• Neubauer S. The failing heart-an engine out of fuel. N Engl J Med 2007, 356, 1140–51.
   PubMed Web of Science ®Google Scholar
• Taegtmeyer H, Golfman L, Sharma S, Razeghi P, van Arsdall M. Linking gene expression to function: metabolic flexibility in the normal and diseased heart. Ann N Y Acad Sci 2004, 1015, 202–13.
   PubMed Web of Science ®Google Scholar
• Alaynick WA, Kondo RP, Xie W, He W, Dufour CR, Downes M, Jonker JW, Giles W, Naviaux RK, Giguere V, Evans RM. ERRγ directs and maintains the transition to oxidative metabolism in the post-natal heart. Cell Metab 2007, 6, 13–24.
   PubMed Web of Science ®Google Scholar
• Huss JM, Imahashi K-I, Dufour C, Weinheimer CJ, Courtois M, Kovacs A, Giguere V, Murphy E, Kelly DP. The nuclear receptor ERRalpha is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab 2007, 6, 25–37.
   PubMed Web of Science ®Google Scholar
• Kizaki T, Suzuki K, Hitomi Y, Taniguchi N, Saitoh D, Watanabe K, Onoe K, Day NK, Good RA, Ohno H. Uncoupling protein 2 plays an important role in nitric oxide production of lipopolysaccharide-stimulated macrophages. Proc Natl Acad Sci U S A 2002, 99, 9392–7.
   PubMed Web of Science ®Google Scholar
• Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, Alves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, Ricquier D. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 2000, 26, 435–9.
   PubMed Web of Science ®Google Scholar
• Tremblay AM, Dufour CR, Ghahremani M, Reudelhuber TL, Giguere V. Physiological genomics identifies estrogen-related receptor alpha as a regulator of renal sodium and potassium homeostasis and the renin–angiotensin pathway. Mol Endocrinol 2010, 24, 22–32.
   PubMedGoogle Scholar
• Stein RA, McDonnell DP. Estrogen-related receptor α as a therapeutic target in cancer. Endocr Relat Cancer 2006, 13, S25–32.
   Web of Science ®Google Scholar
• Kraus RJ, Ariazi EA, Farrell ML, Mertz JE. Estrogen-related receptor alpha 1 actively antagonizes estrogen receptor-regulated transcription in MCF-7 mammary cells. J Biol Chem 2002, 277, 24826–34.
   PubMed Web of Science ®Google Scholar
• Ariazi EA, Clark GM, Mertz JE. Estrogen-related receptor alpha and estrogen-related receptor gamma associate with unfavorable and favorable biomarkers, respectively, in human breast cancer. Cancer Res 2002, 62, 6510–8.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Miki Y, Moriya T, Shimada N, Ishida T, Hirakawa H, Ohuchi N, Sasano H. Estrogen-related receptor alpha in human breast carcinoma as a potent prognostic factor. Cancer Res 2004, 64, 4670–6.
   PubMed Web of Science ®Google Scholar
• Sun P, Sehouli J, Denkert C, Mustea A, Könsgen D, Koch I, Wei L, Lichtenegger W. Expression of estrogen receptor-related receptors, a subfamily of orphan nuclear receptors, as new tumor biomarkers in ovarian cancer cells. J Mol Med 2005, 83, 457–67.
   PubMed Web of Science ®Google Scholar
• Fujimura T, Takahashi S, Urano T, Kumagai J, Ogushi T, Horie-Inoue K, Ouchi Y, Kitamura T, Muramatsu M, Inoue S. Increased expression of estrogen-related receptor alpha (ERRalpha) is a negative prognostic predictor in human prostate cancer. Int J Cancer 2007, 120, 2325–30.
   PubMed Web of Science ®Google Scholar
• Lu D, Kiriyama Y, Lee KY, Giguère V. Transcriptional regulation of the estrogen-inducible pS2 breast cancer marker gene by the ERR family of orphan nuclear receptors. Cancer Res 2001, 61, 6755–61.
   PubMed Web of Science ®Google Scholar
• Bonnelye E, Merdad L, Kung V, Aubin JE. The orphan nuclear estrogen receptor-related receptor alpha (ERRalpha) is expressed throughout osteoblast differentiation and regulates bone formation in vitro. J Cell Biol 2001, 153, 971–84.
   PubMed Web of Science ®Google Scholar
• Cornish J, Callon KE, Naot D, Palmano KP, Banovic T, Bava U, Watson M, Lin JM, Tong PC, Chen Q, Chan VA, Reid HE, Fazzalari N, Baker HM, Baker EN, Haggarty NW, Grey AB, Reid IR. Lactoferrin is a potent regulator of bone cell activity and increases bone formation in vivo. Endocrinology 2004, 145, 4366–74.
   PubMed Web of Science ®Google Scholar
• Kamei Y, Lwin H, Saito K, Yokoyama T, Yoshiike N, Ezaki O, Tanaka H. The 2.3 genotype of ESRRA23 of the ERRα gene is associated with a higher BMI than the 2.2 genotype. Obes Res 2005, 13, 1843–4.
   PubMedGoogle Scholar
• Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science 2005, 307, 384–7.
   PubMed Web of Science ®Google Scholar
• Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. PGC-1alpha responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003, 34, 267–73.
   PubMed Web of Science ®Google Scholar