Estrogen-related receptor-α coordinates transcriptional programs essential for exercise tolerance and muscle fitness

Molecular Endocrinology

Volumn 28, Issue 12, 2014, Pages 2060-2071

  Perry, Marie Claude ^a,b   Dufour, Catherine R ^a   Tam, Ingrid S ^a,b   B’chir, Wafa ^a   Giguère, Vincent ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RELATED RECEPTOR ALPHA; ERRALPHA ESTROGEN-RELATED RECEPTOR; ESTROGEN RECEPTOR;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; ENERGY TRANSFER; ENERGY YIELD; EXERCISE TOLERANCE; FEMALE; FITNESS; GENE EXPRESSION PROFILING; MALE; METABOLOMICS; MOUSE; MUSCLE CELL; MUSCLE EXERCISE; MUSCLE FUNCTION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; REGULATORY MECHANISM; SKELETAL MUSCLE; TREADMILL EXERCISE; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; EXERCISE TOLERANCE; FEMALE; MALE; MICE, KNOCKOUT; MUSCLE, SKELETAL; RECEPTORS, ESTROGEN;

EID: 84914121272     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1281     Document Type: Article

References (47)

1. Booth FW, Thomason DB. Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev. 1991;71:541-585.
2. Hawley JA, Holloszy JO. Exercise: it’s the real thing! Nutr Rev. 2009;67:172-178.
3. Yan Z, Okutsu M, Akhtar YN, Lira VA. Regulation of exerciseinduced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol. 2011;110:264-274.
4. Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev. 2011;91:1447-1531.
5. Giguère V, Yang N, Segui P, Evans RM. Identification of a new class of steroid hormone receptors. Nature. 1988;331:91-94.
6. Deblois G, Giguère V. Functional and physiological genomics of estrogen-related receptors (ERRs) in health and disease. Biochim Biophys Acta. 2011;1812:1032-1040.
7. Eichner LJ, Giguère V. Estrogen related receptors (ERRs): a new dawn in the control of mitochondrial gene networks. Mitochondrion. 2011;11:544-552.
8. Villena JA, Kralli A. ERRalpha: a metabolic function for the oldest orphan. Trends Endocrinol Metab. 2008;19:269-276.
9. Sladek R, Bader JA, Giguère V. The orphan nuclear receptor estrogen-related receptor alpha is a transcriptional regulator of the human medium-chain acyl coenzyme A dehydrogenase gene. Mol Cell Biol. 1997;17:5400-5409.
10. 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;126:789-799.
11. Ichida M, Nemoto S, Finkel T. Identification of a specific molecular repressor of the peroxisome proliferator-activated receptor γ coactivator-1 alpha (PGC-1alpha). J Biol Chem. 2002;277:50991-50995.
12. Villena JA, Hock MB, Chang WY, Barcas JE, Giguère V, Kralli A. Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc Natl Acad Sci U S A. 2007;104: 1418-1423.
13. Huss JM, Imahashi K, Dufour CR, et al. The nuclear receptor ERRalpha is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab. 2007;6:25-37.
14. Dufour CR, Wilson BJ, Huss JM, et al. Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and gamma. Cell Metab. 2007;5:345-356.
15. Giguère V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev. 2008;29:677-696.
16. Deblois G, Giguère V. Oestrogen-related receptors in breast cancer: control of cellular metabolism and beyond. Nat Rev Cancer. 2013; 13:27-36.
17. Murray J, Huss JM. Estrogen-related receptor α regulates skeletal myocyte differentiation via modulation of the ERK MAP kinase pathway. Am J Physiol Cell Physiol. 2011;301:C630-C645.
18. Shao D, Liu Y, Liu X, et al. PGC-1 beta-regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERR alpha. Mitochondrion. 2010;10:516-527.
19. Wang SC, Myers S, Dooms C, Capon R, Muscat GE. An ERRβ/γ agonist modulates GRalpha expression, and glucocorticoid responsive gene expression in skeletal muscle cells. Mol Cell Endocrinol. 2010;315:146-152.
20. Luo J, Sladek R, Carrier J, Bader JA, Richard D, Giguère V. Reduced fat mass in mice lacking orphan nuclear receptor estrogenrelated receptor alpha. Mol Cell Biol. 2003;23:7947-7956.
21. Yoshioka M, Boivin A, Bolduc C, St-Amand J. Gender difference of androgen actions on skeletal muscle transcriptome. J Mol Endocrinol. 2007;39:119-133.
22. Patch RJ, Searle LL, Kim AJ, et al. Identification of diaryl etherbased ligands for estrogen-related receptor α as potential antidiabetic agents. J Med Chem. 2011;54:788-808.
23. Dufour CR, Levasseur MP, Pham NH, et al. Genomic convergence among ERRα, PROX1, and BMAL1 in the control of metabolic clock outputs. PLoS Genet. 2011;7:e1002143.
24. Herzog B, Cardenas J, Hall RK, et al. Estrogen-related receptor alpha is a repressor of phosphoenolpyruvate carboxykinase gene transcription. J Biol Chem. 2006;281:99-106.
25. Gleeson TT, Putnam RW, Bennett AF. Histochemical, enzymatic, and contractile properties of skeletal muscle fibers in the lizard Dipsosaurus dorsalis. J Exp Zool. 1980;214:293-302.
26. Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17:162-184.
27. Austin S, St-Pierre J. PGC1α and mitochondrial metabolism- emerging concepts and relevance in ageing and neurodegenerative disorders. J Cell Sci. 2012;125:4963-4971.
28. Huss JM, Kopp RP, Kelly DP. Peroxisome proliferator-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiacenriched nuclear receptors estrogen-related receptor-alpha and -gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J Biol Chem. 2002;277:40265-40274.
29. Baar K, Wende AR, Jones TE, et al. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002;16:1879-1886.
30. Yoshioka M, Doucet E, St-Pierre S, et al. Impact of high-intensity exercise on energy expenditure, lipid oxidation and body fatness. Int J Obes Relat Metab Disord. 2001;25:332-339.
31. Miller CJ, Gounder SS, Kannan S, et al. Disruption of Nrf2/ARE signaling impairs antioxidant mechanisms and promotes cell degradation pathways in aged skeletal muscle. Biochim Biophys Acta. 2012;1822:1038-1050.
32. Muthusamy VR, Kannan S, Sadhaasivam K, et al. Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium. Free Radic Biol Med. 2012;52: 366-376.
33. Waddell DS, Baehr LM, van den Brandt J, et al. The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab. 2008;295:E785-E797.
34. Masiero E, Agatea L, Mammucari C, et al. Autophagy is required to maintain muscle mass. Cell Metab. 2009;10:507-515.
35. Murton AJ, Constantin D, Greenhaff PL. The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy. Biochim Biophys Acta. 2008;1782:730-743.
36. Gustafsson T, Kraus WE. Exercise-induced angiogenesis-related growth and transcription factors in skeletal muscle, and their modification in muscle pathology. Front Biosci. 2001;6:D75-D89.
37. Fan W, Atkins AR, Yu RT, Downes M, Evans RM. Road to exercise mimetics: targeting nuclear receptors in skeletal muscle. J Mol Endocrinol. 2013;51:T87-T100.
38. Charest-Marcotte A, Dufour CR, Wilson BJ, et al. The homeobox protein Prox1 is a negative modulator of ERRα/PGC-1α bioenergetic functions. Genes Dev. 2010;24:537-542.
39. Chaveroux C, Eichner LJ, Dufour CR, et al. Molecular and genetic crosstalks between mTOR and ERRα are key determinants of rapamycin-induced nonalcoholic fatty liver. Cell Metab. 2013;17: 586-598.
40. Zechner C, Lai L, Zechner JF, et al. Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity. Cell Metab. 2010;12:633-642.
41. Sonoda J, Laganière J, Mehl IR, et al. Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense. Genes Dev. 2007;21:1909-1920.
42. Tremblay AM, Dufour CR, Ghahremani M, Reudelhuber TL, Giguère 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.
43. Summermatter S, Santos G, Pérez-Schindler J, Handschin C. Skeletal muscle PGC-1α controls whole-body lactate homeostasis through estrogen-related receptor α-dependent activation of LDH B and repression of LDH A. Proc Natl Acad Sci U S A. 2013;110: 8738-8743.
44. Handschin C, Chin S, Li P, et al. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha musclespecific knock-out animals. J Biol Chem. 2007;282:30014-30021.
45. Arany Z, Foo SY, Ma Y, et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature. 2008;451:1008-1012.
46. Narkar VA, Fan W, Downes M, et al. Exercise and PGC-1α-independent synchronization of type I muscle metabolism and vasculature by ERRα. Cell Metab. 2011;13:283-293.
47. Alaynick WA, Kondo RP, Xie W, et al. ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab. 2007;6:13-24.