The orphan nuclear receptor Nur77 Is a determinant of myofiber size and muscle mass in mice

Molecular and Cellular Biology

Volumn 35, Issue 7, 2015, Pages 1125-1138

  Tontonoz, Peter ^a,b   Cortez Toledo, Omar ^c   Wroblewski, Kevin ^a   Hong, Cynthia ^a   Lim, Laura ^c   Carranza, Rogelio ^c   Conneely, Orla ^d   Metzger, Daniel ^e   Chao, Lily C ^a,c,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e Centre de Recherche Interdisciplinaire en Biologie   (France)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; MAMMALIAN TARGET OF RAPAMYCIN; NUCLEAR RECEPTOR NUR77; PROTEIN; PROTEIN KINASE B; S6K PROTEIN; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHRL1; TRIM63 PROTEIN; UNCLASSIFIED DRUG; FBXO32 PROTEIN, MOUSE; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; MTOR PROTEIN, MOUSE; MUSCLE PROTEIN; TARGET OF RAPAMYCIN KINASE; TRIM63 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GROWTH REGULATION; MALE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE MASS; MYOFIBER SIZE; MYOTUBE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; SKELETAL MUSCLE; TISSUE DIFFERENTIATION; ANIMAL; C57BL MOUSE; CELL CULTURE; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

MUS;

ANIMALS; CELLS, CULTURED; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUTATION; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TOR SERINE-THREONINE KINASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84924873977     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00715-14     Document Type: Article

References (64)

1. von Haehling S, Anker SD. 2012. Cachexia as major underestimated unmet medical need: facts and numbers. Int J Cardiol 161:121-123. http://dx.doi.org/10.1016/j.ijcard.2012.09.213.
2. Srikanthan P, Hevener AL, Karlamangla AS. 2010. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One 5:e10805. http://dx.doi.org/10.1371/journal.pone.0010805.
3. Srikanthan P, Karlamangla AS. 2011. Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 96:2898-2903. http://dx.doi.org/10.1210/jc.2011-0435.
4. Bauman WA, Spungen AM. 1994. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 43:749-756. http://dx.doi.org/10.1016/0026-0495(94)90126-0.
5. Ryall JG, Church JE, Lynch GS. 2010. Novel role for ss-adrenergic signalling in skeletal muscle growth, development and regeneration. Clin Exp Pharmacol Physiol 37:397-401. http://dx.doi.org/10.1111/j.1440-1681.2009.05312.x.
6. Egerman MA, Glass DJ. 2014. Signaling pathways controlling skeletal muscle mass. Crit Rev Biochem Mol Biol 49:59-68. http://dx.doi.org/10.3109/10409238.2013.857291.
7. Gundersen K. 2011. Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 86:564-600. http://dx.doi.org/10.1111/j.1469-185X.2010.00161.x.
8. Duchene S, Audouin E, Crochet S, Duclos MJ, Dupont J, Tesseraud S. 2008. Involvement of the ERK1/2 MAPK pathway in insulin-induced S6K1 activation in avian cells. Domest Anim Endocrinol 34:63-73. http://dx.doi.org/10.1016/j.domaniend.2006.11.001.
9. Haddad F, Adams GR. 2004. Inhibition of MAP/ERK kinase prevents IGF-I-induced hypertrophy in rat muscles. J Appl Physiol 96:203-210. http://dx.doi.org/10.1152/japplphysiol.00856.2003.
10. Ryder JW, Fahlman R, Wallberg-Henriksson H, Alessi DR, Krook A, Zierath JR. 2000. Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. Involvement off the mitogenand stress-activated protein kinase 1. J Biol Chem 275:1457-1462. http://dx.doi.org/10.1074/jbc.275.2.1457.
11. Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, Barron N, McCaffrey N, Moyna NM, Zierath JR, O'Gorman DJ. 2010. Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor γ coactivator-1α mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol 588:1779-1790. http://dx.doi.org/10.1113/jphysiol.2010.188011.
12. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM. 2012. A PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151:1319-1331. http://dx.doi.org/10.1016/j.cell.2012.10.050.
13. Ruegg MA, Glass DJ. 2011. Molecular mechanisms and treatment options for muscle wasting diseases. Annu Rev Pharmacol Toxicol 51:373-395. http://dx.doi.org/10.1146/annurev-pharmtox-010510-100537.
14. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ashby M, Ling N, Smith H, Sharma M, Kambadur R. 2006. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-κB-independent, FoxO1-dependent mechanism. J Cell Physiol 209:501-514. http://dx.doi.org/10.1002/jcp.20757.
15. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. 2004. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395-403. http://dx.doi.org/10.1016/S1097-2765(04)00211-4.
16. Helbling JC, Minni AM, Pallet V, Moisan MP. 2014. Stress and glucocorticoid regulation of NR4A genes in mice. J Neurosci Res 92:825-834. http://dx.doi.org/10.1002/jnr.23366.
17. Maxwell MA, Muscat GE. 2006. The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl Recept Signal 4:e002. http://dx.doi.org/10.1621/nrs.04002.
18. 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. http://dx.doi.org/10.1210/me.2007-0169.
19. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. 2005. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J 19:1498-1500. http://dx.doi.org/10.1096/fj.04-3149fje.
20. 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. http://dx.doi.org/10.2337/db09-0763.
21. Chao LC, Wroblewski K, Ilkayeva OR, Stevens RD, Bain J, Meyer GA, Schenk S, Martinez L, Vergnes L, Narkar VA, Drew BG, Hong C, Boyadjian R, Hevener AL, Evans RM, Reue K, Spencer MJ, Newgard CB, Tontonoz P. 2012. Skeletal muscle Nur77 expression enhances oxidative metabolism and substrate utilization. J Lipid Res 53:2610-2619. http://dx.doi.org/10.1194/jlr. M029355.
22. Pearen MA, Eriksson NA, Fitzsimmons RL, Goode JM, Martel N, Andrikopoulos S, Muscat GE. 2012. The nuclear receptor, Nor-1, markedly increases type II oxidative muscle fibers and resistance to fatigue. Mol Endocrinol 26:372-384. http://dx.doi.org/10.1210/me.2011-1274.
23. Sekiya T, Kashiwagi I, Yoshida R, Fukaya T, Morita R, Kimura A, Ichinose H, Metzger D, Chambon P, Yoshimura A. 2013. Nr4a receptors are essential for thymic regulatory T cell development and immune homeostasis. Nat Immunol 14:230-237. http://dx.doi.org/10.1038/ni.2520.
24. Ponnio T, Burton Q, Pereira FA, Wu DK, Conneely OM. 2002. The nuclear receptor Nor-1 is essential for proliferation of the semicircular canals of the mouse inner ear. Mol Cell Biol 22:935-945. http://dx.doi.org/10.1128/MCB.22.3.935-945.2002.
25. Chao LC, Soto E, Hong C, Ito A, Pei L, Chawla A, Conneely OM, Tangirala RK, Evans RM, Tontonoz P. 2013. Bone marrow NR4A expression is not a dominant factor in the development of atherosclerosis or macrophage polarization in mice. J Lipid Res 54:806-815. http://dx.doi.org/10.1194/jlr. M034157.
26. Rando TA, Blau HM. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 125:1275-1287. http://dx.doi.org/10.1083/jcb.125.6.1275.
27. Frey N, Frank D, Lippl S, Kuhn C, Kogler H, Barrientos T, Rohr C, Will R, Muller 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. http://dx.doi.org/10.1172/JCI36277.
28. Lach-Trifilieff E, Minetti GC, Sheppard K, Ibebunjo C, Feige JN, Hartmann S, Brachat S, Rivet H, Koelbing C, Morvan F, Hatakeyama S, Glass DJ. 2014. An antibody blocking activin type II receptors induces strong skeletal muscle hypertrophy and protects from atrophy. Mol Cell Biol 34:606-618. http://dx.doi.org/10.1128/MCB.01307-13.
29. Pearen MA, Goode JM, Fitzsimmons RL, Eriksson NA, Thomas GP, Cowin GJ, Wang SC, Tuong ZK, Muscat GE. 2013. Transgenic musclespecific Nor-1 expression regulates multiple pathways that effect adiposity, metabolism, and endurance. Mol Endocrinol 27:1897-1917. http://dx.doi.org/10.1210/me.2013-1205.
30. 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. http://dx.doi.org/10.1038/nm1471.
31. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL, Rosenthal N. 2001. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27:195-200. http://dx.doi.org/10.1038/84839.
32. Stewart CE, Pell JM. 2010. Point:counterpoint: IGF is/is not the major physiological regulator of muscle mass. Point: IGF is the major physiological regulator of muscle mass. J Appl Physiol 108:1820-1824. http://dx.doi.org/10.1152/japplphysiol.01246.2009.
33. Shavlakadze T, Davies M, White JD, Grounds MD. 2004. Early regeneration of whole skeletal muscle grafts is unaffected by overexpression of IGF-1 in MLC/mIGF-1 transgenic mice. J Histochem Cytochem 52:873-883. http://dx.doi.org/10.1369/jhc.3A6177.2004.
34. Kardon G, Heanue TA, Tabin CJ. 2002. Pax3 and Dach2 positive regulation in the developing somite. Dev Dyn 224:350-355. http://dx.doi.org/10.1002/dvdy.10107.
35. Baehr LM, Furlow JD, Bodine SC. 2011. Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J Physiol 589:4759-4776. http://dx.doi.org/10.1113/jphysiol.2011.212845.
36. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. 2001. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704-1708. http://dx.doi.org/10.1126/science.1065874.
37. Labeit S, Kohl CH, Witt CC, Labeit D, Jung J, Granzier H. 2010. Modulation of muscle atrophy, fatigue and MLC phosphorylation by MuRF1 as indicated by hindlimb suspension studies on MuRF1-KO mice. J Biomed Biotechnol 2010:693741. http://dx.doi.org/10.1155/2010/693741.
38. Bhatnagar S, Mittal A, Gupta SK, Kumar A. 2012. TWEAK causes myotube atrophy through coordinated activation of ubiquitinproteasome system, autophagy, and caspases. J Cell Physiol 227:1042-1051. http://dx.doi.org/10.1002/jcp.22821.
39. McPherron AC, Lawler AM, Lee SJ. 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83-90. http://dx.doi.org/10.1038/387083a0.
40. Shi J, Luo L, Eash J, Ibebunjo C, Glass DJ. 2011. The SCF-Fbxo40 complex induces IRS1 ubiquitination in skeletal muscle, limiting IGF1 signaling. Dev Cell 21:835-847. http://dx.doi.org/10.1016/j.devcel.2011.09.011.
41. Ye J, Zhang Y, Xu J, Zhang Q, Zhu D. 2007. FBXO40, a gene encoding a novel muscle-specific F-box protein, is upregulated in denervation-related muscle atrophy. Gene 404:53-60. http://dx.doi.org/10.1016/j.gene.2007.08.020.
42. Gomes AV, Waddell DS, Siu R, Stein M, Dewey S, Furlow JD, Bodine SC. 2012. Upregulation of proteasome activity in muscle RING finger 1-null mice following denervation. FASEB J 26:2986-2999. http://dx.doi.org/10.1096/fj.12-204495.
43. Ovcharenko I, Nobrega MA, Loots GG, Stubbs L. 2004. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res 32:W280-W286. http://dx.doi.org/10.1093/nar/gkh355.
44. Dinchuk JE, Cao C, Huang F, Reeves KA, Wang J, Myers F, Cantor GH, Zhou X, Attar RM, Gottardis M, Carboni JM. 2010. Insulin receptor (IR) pathway hyperactivity in IGF-IR null cells and suppression of downstream growth signaling using the dual IGF-IR/IR inhibitor, BMS-754807. Endocrinology 151:4123-4132. http://dx.doi.org/10.1210/en.2010-0032.
45. Yamamoto Y, Hoshino Y, Ito T, Nariai T, Mohri T, Obana M, Hayata N, Uozumi Y, Maeda M, Fujio Y, Azuma J. 2008. Atrogin-1 ubiquitin ligase is upregulated by doxorubicin via p38-MAP kinase in cardiac myocytes. Cardiovasc Res 79:89-96. http://dx.doi.org/10.1093/cvr/cvn076.
46. Li J, Johnson SE. 2006. ERK2 is required for efficient terminal differentiation of skeletal myoblasts. Biochem Biophys Res Commun 345:1425-1433. http://dx.doi.org/10.1016/j.bbrc.2006.05.051.
47. Sarbassov DD, Jones LG, Peterson CA. 1997. Extracellular signal-regulated kinase-1 and -2 respond differently to mitogenic and differentiative signaling pathways in myoblasts. Mol Endocrinol 11:2038-2047. http://dx.doi.org/10.1210/mend.11.13.0036.
48. Plaisance I, Morandi C, Murigande C, Brink M. 2008. TNF-alpha increases protein content in C2C12 and primary myotubes by enhancing protein translation via the TNF-R1, PI3K, and MEK. Am J Physiol Endocrinol Metab 294:E241-E250. http://dx.doi.org/10.1152/ajpendo.00129.2007.
49. Backs J, Song K, Bezprozvannaya S, Chang S, Olson EN. 2006. CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest 116:1853-1864. http://dx.doi.org/10.1172/JCI27438.
50. McKinsey TA, Zhang CL, Lu J, Olson EN. 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408:106-111. http://dx.doi.org/10.1038/35040593.
51. McKinsey TA, Zhang CL, Olson EN. 2000. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci U S A 97:14400-14405. http://dx.doi.org/10.1073/pnas.260501497.
52. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ. 2009. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296: C1258-C1270. http://dx.doi.org/10.1152/ajpcell.00105.2009.
53. Mullican SE, Zhang S, Konopleva M, Ruvolo V, Andreeff M, Milbrandt J, Conneely OM. 2007. Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat Med 13:730-735. http://dx.doi.org/10.1038/nm1579.
54. Wu CL, Kandarian SC, Jackman RW. 2011. Identification of genes that elicit disuse muscle atrophy via the transcription factors p50 and Bcl-3. PLoS One 6:e16171. http://dx.doi.org/10.1371/journal.pone.0016171.
55. Lu J, McKinsey TA, Nicol RL, Olson EN. 2000. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci U S A 97:4070-4075. http://dx.doi.org/10.1073/pnas.080064097.
56. Lu J, McKinsey TA, Zhang CL, Olson EN. 2000. Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell 6:233-244. http://dx.doi.org/10.1016/S1097-2765(00)00025-3.
57. Backs J, Worst BC, Lehmann LH, Patrick DM, Jebessa Z, Kreusser MM, Sun Q, Chen L, Heft C, Katus HA, Olson EN. 2011. Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4. J Cell Biol 195:403-415. http://dx.doi.org/10.1083/jcb.201105063.
58. Liu Y, Schneider MF. 2013. Opposing HDAC4 nuclear fluxes due to phosphorylation by ß-adrenergic activated protein kinase A or by activity or Epac activated CaMKII in skeletal muscle fibres. J Physiol 591:3605-3623. http://dx.doi.org/10.1113/jphysiol.2013.256263.
59. Maxwell MA, Cleasby ME, Harding A, Stark A, Cooney GJ, Muscat GE. 2005. Nur77 regulates lipolysis in skeletal muscle cells. Evidence for crosstalk between the beta-adrenergic and an orphan nuclear hormone receptor pathway. J Biol Chem 280:12573-12584. http://dx.doi.org/10.1074/jbc. M409580200.
60. Grefte S, Kuijpers-Jagtman AM, Torensma R, Von den Hoff JW. 2007. Skeletal muscle development and regeneration. Stem Cells Dev 16:857-868. http://dx.doi.org/10.1089/scd.2007.0058.
61. Chao LC, Bensinger SJ, Villanueva CJ, Wroblewski K, Tontonoz P. 2008. Inhibition of adipocyte differentiation by Nur77, Nurr1, and Nor1. Mol Endocrinol 22:2596-2608. http://dx.doi.org/10.1210/me.2008-0161.
62. Tessem JS, Moss LG, Chao LC, Arlotto M, Lu D, Jensen MV, Stephens SB, Tontonoz P, Hohmeier HE, Newgard CB. 2014. Nkx6.1 regulates islet beta-cell proliferation via Nr4a1 and Nr4a3 nuclear receptors. Proc Natl Acad Sci U S A 111:5242-5247. http://dx.doi.org/10.1073/pnas.1320953111.
63. D'Souza DM, Al-Sajee D, Hawke TJ. 2013. Diabetic myopathy: impact of diabetes mellitus on skeletal muscle progenitor cells. Front Physiol 4:379. http://dx.doi.org/10.3389/fphys.2013.00379.
64. Woo M, Isganaitis E, Cerletti M, Fitzpatrick C, Wagers AJ, Jimenez-Chillaron J, Patti ME. 2011. Early life nutrition modulates muscle stem cell number: implications for muscle mass and repair. Stem Cells Dev 20:1763-1769. http://dx.doi.org/10.1089/scd.2010.0349.