The nuclear receptor, Nor-1, markedly increases type II oxidative muscle fibers and resistance to fatigue

Molecular Endocrinology

Volumn 26, Issue 3, 2012, Pages 372-384

  Pearen, Michael A ^a   Eriksson, Natalie A ^a   Fitzsimmons, Rebecca L ^a   Goode, Joel M ^a   Martel, Nick ^a   Andrikopoulos, Sofianos ^b   Muscat, George E O ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 5; MITOCHONDRIAL DNA; MYOCYTE ENHANCER FACTOR 2; MYOGLOBIN; MYOSIN; MYOSIN II; MYOSIN IIA; MYOSIN IIB; MYOSIN IIX; NUCLEAR RECEPTOR NR4A3; OXIDOREDUCTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENSITY; ELECTRON TRANSPORT; ENDURANCE; GLUCOSE TOLERANCE; IN VIVO STUDY; MALE; MOUSE; MUSCLE FATIGUE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; BLOOD GLUCOSE; GENES, MITOCHONDRIAL; HISTONE DEACETYLASES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; MUSCLE FIBERS, FAST-TWITCH; MYOGLOBIN; MYOSIN HEAVY CHAINS; NAD; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 3; OXIDATION-REDUCTION; PHOSPHORYLATION; PHYSICAL ENDURANCE; PROTEIN ISOFORMS; REAL-TIME POLYMERASE CHAIN REACTION; SUCCINATE DEHYDROGENASE; TRANSCRIPTION, GENETIC;

MUS;

EID: 84857487126     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1274     Document Type: Article

References (70)

1. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ 2001 Nuclear receptors and lipid physiology: opening the X-files. Science 294: 1866-1870
2. Wilson TE, Fahrner TJ, Johnston M, Milbrandt J 1991 Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252:1296-1300
3. Wansa KD, Harris JM, Yan G, Ordentlich P, Muscat GE 2003 The AF-1 domain of the orphan nuclear receptor NOR-1 mediates trans-activation, coactivator recruitment, and activation by the purine anti-metabolite 6-mercaptopurine. J Biol Chem 278:24776-24790
4. Chintharlapalli S, Burghardt R, Papineni S, Ramaiah S, Yoon K, Safe S 2005 Activation of Nur77 by selected 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes induces apoptosis through nuclear pathways. J Biol Chem 280:24903-24914
5. Zhan Y, Du X, Chen H, Liu J, Zhao B, Huang D, Li G, Xu Q, Zhang M, Weimer BC, Chen D, Cheng Z, Zhang L, Li Q, Li S, Zheng Z, Song S, Huang Y, Ye Z, Su W, Lin SC, Shen Y, Wu Q 2008 Cytosporone B is an agonist for nuclear orphan receptor Nur77. Nat Chem Biol 4:548-556
6. Kagaya S, Ohkura N, Tsukada T, Miyagawa M, Sugita Y, Tsujimoto G, Matsumoto K, Saito H, Hashida R 2005 Prostaglandin A2 acts as a transactivator for NOR1 (NR4A3) within the nuclear receptor superfamily. Biol Pharm Bull 28:1603-1607
7. Hintermann S, Chiesi M, von Krosigk U, Mathé D, Felber R, Hengerer B 2007 Identification of a series of highly potent activators of the Nurr1 signaling pathway. Bioorg Med Chem Lett 17:193-196
8. Dubois C, Hengerer B, Mattes H 2006 Identification of a potent agonist of the orphan nuclear receptor Nurr1. ChemMedChem 1:955-958
9. Pearen MA, Muscat GE 2010 Minireview: nuclear hormone receptor 4A signaling: implications for metabolic disease. Mol Endocrinol 24:1891-1903
10. Pearen MA, Myers SA, Raichur S, Ryall JG, Lynch GS, Muscat GE 2008 The orphan nuclear receptor, NOR-1, a target of β-adrenergic signaling, regulates gene expression that controls oxidative metabolism in skeletal muscle. Endocrinology 149:2853-2865
11. Maxwell MA, Cleasby ME, Harding A, Stark A, Cooney GJ, Muscat GE 2005 Nur77 regulates lipolysis in skeletal muscle cells. Evidence for cross-talk between the β-adrenergic and an orphan nuclear hormone receptor pathway. J Biol Chem 280:12573-12584
12. Chao LC, Zhang Z, Pei L, Saito T, Tontonoz P, Pilch PF 2007 Nur77 coordinately regulates expression of genes linked to glucose metabolism in skeletal muscle. Mol Endocrinol 21:2152-2163
13. Kanzleiter T, Schneider T, Walter I, Bolze F, Eickhorst C, Heldmaier G, Klaus S, Klingenspor M 2005 Evidence for Nr4a1 as a cold-induced effector of brown fat thermogenesis. Physiol Genomics 24:37-44
14. Kumar N, Liu D, Wang H, Robidoux J, Collins S 2008 Orphan nuclear receptor NOR-1 enhances 3',5'-cyclic adenosine 5'-monophosphate-dependent uncoupling protein-1 gene transcription. Mol Endocrinol 22:1057-1064
15. Roche E, Buteau J, Aniento I, Reig JA, Soria B, Prentki M 1999 Palmitate and oleate induce the immediate-early response genes c-fos and nur-77 in the pancreatic β-cell line INS-1. Diabetes 48: 2007-2014
16. Susini S, Roche E, Prentki M, Schlegel W 1998 Glucose and glucoincretin peptides synergize to induce c-fos, c-jun, junB, zif-268, and nur-77 gene expression in pancreatic β (INS-1) cells. FASEB J 12: 1173-1182
17. Wu X, Wang J, Cui X, Maianu L, Rhees B, Rosinski J, So WV, Willi SM, Osier MV, Hill HS, Page GP, Allison DB, Martin M, Garvey WT 2007 The effect of insulin on expression of genes and biochemical pathways in human skeletal muscle. Endocrine 31:5-17
18. Rius J, Martínez-González J, Crespo J, Badimon L 2004 Involvement of neuron-derived orphan receptor-1 (NOR-1) in LDL-induced mitogenic stimulus in vascular smooth muscle cells: role of CREB. Arterioscler Thromb Vasc Biol 24:697-702
19. Wang SC, Myers SA, Eriksson NA, Fitzsimmons RL, Muscat GE 2011 Nr4a1 siRNA expression attenuates α-MSH regulated gene expression in 3T3-L1 adipocytes. Mol Endocrinol 25:291-306
20. Fu Y, Luo L, Luo N, Zhu X, Garvey WT 2007 NR4A orphan nuclear receptors modulate insulin action and the glucose transport system: potential role in insulin resistance. J Biol Chem 282:31525-31533
21. Pearen MA, Ryall JG, Maxwell MA, Ohkura N, Lynch GS, Muscat GE 2006 The orphan nuclear receptor, NOR-1, is a target of β-adrenergic signaling in skeletal muscle. Endocrinology 147:5217-5227
22. Chao LC, Wroblewski K, Zhang Z, Pei L, Vergnes L, Ilkayeva OR, Ding SY, Reue K, Watt MJ, Newgard CB, Pilch PF, Hevener AL, Tontonoz P 2009 Insulin resistance and altered systemic glucose metabolism in mice lacking Nur77. Diabetes 58:2788-2796
23. Kanzleiter T, Wilks D, Preston E, Ye J, Frangioudakis G, Cooney GJ 2009 Regulation of the nuclear hormone receptor nur77 in muscle: influence of exercise-activated pathways in vitro and obesity in vivo. Biochim Biophys Acta 1792:777-782
24. Pols TW, Bonta PI, de Vries CJ 2007 NR4A nuclear orphan receptors: protective in vascular disease? Curr Opin Lipidol 18:515-520
25. Pei L, Waki H, Vaitheesvaran B, Wilpitz DC, Kurland IJ, Tontonoz P 2006 NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat Med 12:1048-1055
26. Owen OE, Reichard GAJ, Boden G, Patel MS, Trapp VE 1978 Interrelationships among key tissues in the utilization of metabolic substrate. Adv Mod Nutr 2:517-550
27. Zurlo F, Larson K, Bogardus C, Ravussin E 1990 Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 86:1423-1427
28. Muscat GE, Kedes L 1987 Multiple 5'-flanking regions of the human α-skeletal actin gene synergistically modulate muscle-specific expression. Mol Cell Biol 7:4089-4099
29. Brennan KJ, Hardeman EC 1993 Quantitative analysis of the human α-skeletal actin gene in transgenic mice. J Biol Chem 268:719-725
30. Li Y, Lazar MA 2002 Differential gene regulation by PPARγ agonist and constitutively active PPARγ2. Mol Endocrinol 16:1040-1048
31. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM 2004 Regulation of muscle fiber type and running endurance by PPARδ. PLoS Biol 2:e294
32. Noshiro M, Usui E, Kawamoto T, Sato F, Nakashima A, Ueshima T, Honda K, Fujimoto K, Honma S, Honma K, Makishima M, Kato Y 2009 Liver X receptors (LXRα and LXRβ) are potent regulators for hepatic Dec1 expression. Genes Cells 14:29-40
33. Suino-Powell K, Xu Y, Zhang C, Tao YG, Tolbert WD, Simons Jr SS, Xu HE 2008 Doubling the size of the glucocorticoid receptor ligand binding pocket by deacylcortivazol. Mol Cell Biol 28:1915-1923
34. Rangwala SM, Wang X, Calvo JA, Lindsley L, Zhang Y, Deyneko G, Beaulieu V, Gao J, Turner G, Markovits J 2010 Estrogen-related receptor γ is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285:22619-22629
35. Fazeli S, Wells DJ, Hobbs C, Walsh FS 1996 Altered secondary myogenesis in transgenic animals expressing the neural cell adhesion molecule under the control of a skeletal muscle α-actin promoter. J Cell Biol 135:241-251
36. Raichur S, Fitzsimmons RL, Myers SA, Pearen MA, Lau P, Eriksson N, Wang SM, Muscat GE 2010 Identification and validation of the pathways and functions regulated by the orphan nuclear receptor, RORα1, in skeletal muscle. Nucleic Acids Res 38:4296-4312
37. Pearce NJ, Arch JR, Clapham JC, Coghlan MP, Corcoran SL, Lister CA, Llano A, Moore GB, Murphy GJ, Smith SA, Taylor CM, Yates JW, Morrison AD, Harper AJ, Roxbee-Cox L, Abuin A, Wargent E, Holder JC 2004 Development of glucose intolerance in male transgenic mice overexpressing human glycogen synthase kinase-3β on a muscle-specific promoter. Metabolism 53:1322-1330
38. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS 2001 Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20:6414-6423
39. Arany Z, Lebrasseur N, Morris C, Smith E, Yang W, Ma Y, Chin S, Spiegelman BM 2007 The transcriptional coactivator PGC-1β drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5:35-46
40. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM 2002 Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418:797-801
41. Bach D, Pich S, Soriano FX, Vega N, Baumgartner B, Oriola J, Daugaard JR, Lloberas J, Camps M, Zierath JR, Rabasa-Lhoret R, Wallberg-Henriksson H, Laville M, Palacín M, Vidal H, Rivera F, Brand M, Zorzano A 2003 Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J Biol Chem 278:17190-17197
42. Frey N, Frank D, Lippl S, Kuhn C, Kögler H, Barrientos T, Rohr C, Will R, Müller OJ, Weiler H, Bassel-Duby R, Katus HA, Olson EN 2008 Calsarcin-2 deficiency increases exercise capacity in mice through calcineurin/NFAT activation. J Clin Invest 118:3598-3608
43. McKinsey TA, Zhang CL, Lu J, Olson EN 2000 Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408:106-111
44. Knight JD, Kothary R 2011 The myogenic kinome: protein kinases critical to mammalian skeletal myogenesis. Skelet Muscle 1:29
45. Martin M, Kettmann R, Dequiedt F 2007 Class IIa histone deacetylases: regulating the regulators. Oncogene 26:5450-5467
46. Bassel-Duby R, Olson EN 2006 Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75:19-37
47. McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M 2008 AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57:860-867
48. Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, Shaw RJ, Yates 3rd JR, Fischer WH, Thomas JB, Montminy M 2011 A hormone-dependent module regulating energy balance. Cell 145: 596-606
49. Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M, Shaw RJ 2011 Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145:607-621
50. Handschin C 2011 Peroxisome proliferator-activated receptor γ coactivator 1β (PGC-1β) improves skeletal muscle mitochondrial function and insulin sensitivity. Diabetologia 54:1270-1272
51. Blaak EE, Van Baak MA, Kemerink GJ, Pakbiers MT, Heidendal GA, Saris WH 1994 β-Adrenergic stimulation of energy expenditure and forearm skeletal muscle metabolism in lean and obese men. Am J Physiol 267:E306-E315
52. Hagström-Toft E, Enoksson S, Moberg E, Bolinder J, Arner P 1998 β-Adrenergic regulation of lipolysis and blood flow in human skeletal muscle in vivo. Am J Physiol 275:E909-E916
53. Blaak EE 2004 Basic disturbances in skeletal muscle fatty acid metabolism in obesity and type 2 diabetes mellitus. Proc Nutr Soc 63:323-330
54. Fagher B, Liedholm H, Monti M, Moritz U 1986 Thermogenesis in human skeletal muscle as measured by direct microcalorimetry and muscle contractile performance during β-adrenoceptor blockade. Clin Sci 70:435-441
55. Lessard SJ, Rivas DA, Chen ZP, van Denderen BJ, Watt MJ, Koch LG, Britton SL, Kemp BE, Hawley JA 2009 Impaired skeletal muscle β-adrenergic activation and lipolysis are associated with wholebody insulin resistance in rats bred for low intrinsic exercise capacity. Endocrinology 150:4883-4891
56. Szendroedi J, Phielix E, Roden M 13 September 2011 The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol 10.1038/nrendo.2011.138
57. Sadowski I, Ma J, Triezenberg S, Ptashne M 1988 GAL4-VP16 is an unusually potent transcriptional activator. Nature 335:563-564
58. Wansa KD, Muscat GE 2005 TRAP220 is modulated by the antineoplastic agent 6-mercaptopurine, and mediates the activation of the NR4A subgroup of nuclear receptors. J Mol Endocrinol 34: 835-848
59. Pearen MA, Ryall JG, Lynch GS, Muscat GE 2009 Expression profiling of skeletal muscle following acute and chronic β2-adrenergic stimulation: implications for hypertrophy, metabolism and circadian rhythm. BMC Genomics 10:448
60. Crowther LM, Wang SC, Eriksson NA, Myers SA, Murray LA, Muscat GE 2011 Chicken ovalbumin upstream promoter-transcription factor II regulates nuclear receptor, myogenic, and metabolic gene expression in skeletal muscle cells. Physiol Genomics 43:213-227
61. Myers SA, Eriksson N, Burow R, Wang SC, Muscat GE 2009 β-Adrenergic signaling regulates NR4A nuclear receptor and metabolic gene expression in multiple tissues. Mol Cell Endocrinol 309:101-108
62. Bian K, Harari Y, Zhong M, Lai M, Castro G, Weisbrodt N, Murad F 2001 Down-regulation of inducible nitric-oxide synthase (NOS-2) during parasite-induced gut inflammation: a path to identify a selective NOS-2 inhibitor. Mol Pharmacol 59:939-947
63. Abramoff MD, Magalhaes PJ, Ram SJ 2004 Image Processing with ImageJ. Biophotonics Int 11:36-42
64. Jackson KA, Snyder DS, Goodell MA 2004 Skeletal muscle fiberspecific green autofluorescence: potential for stem cell engraftment artifacts. Stem Cells 22:180-187
65. Lucas CA, Kang LH, Hoh JF 2000 Monospecific antibodies against the three mammalian fast limb myosin heavy chains. Biochem Biophys Res Commun 272:303-308
66. Parton RG 1994 Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 42:155-166
67. Rossini K, Rizzi C, Sandri M, Bruson A, Carraro U 1995 Highresolution sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunochemical identification of the 2X and embryonic myosin heavy chains in complex mixtures of isomyosins. Electrophoresis 16:101-104
68. Merril CR, Goldman D, Sedman SA, Ebert MH 1981 Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science 211:1437-1438
69. Smyth GK 2004 Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3
70. Goni R, Garcia P, Foissac ST 2009 The qPCR data statistical analysis. Integromics White Paper (September 2009): 1-9