Muscle ERRγ mitigates Duchenne muscular dystrophy via metabolic and angiogenic reprogramming

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4004-4016

  Matsakas, Antonios ^a   Yadav, Vikas ^a   Lorca, Sabina ^a   Narkar, Vihang ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Estrogen related receptors; Fiber type; Muscle degenerative diseases; Nuclear receptors

Indexed keywords

DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; ESTROGEN RECEPTOR; ESTROGEN RELATED RECEPTOR GAMMA; GLYCOPROTEIN; UNCLASSIFIED DRUG; CREATINE KINASE; ESRRG PROTEIN, MOUSE; UTROPHIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EXERCISE TOLERANCE; FATIGUE; FEMALE; GENE EXPRESSION; HYPOXIA; MALE; METABOLIC REGULATION; MOUSE; MUSCLE BLOOD FLOW; MUSCLE BLOOD VESSEL; MUSCLE CELL; MUSCLE INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SKELETAL MUSCLE; WILD TYPE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

MUS;

ANIMALS; CREATINE KINASE; DYSTROPHIN-ASSOCIATED PROTEIN COMPLEX; GENE EXPRESSION REGULATION; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; RECEPTORS, ESTROGEN; UTROPHIN;

EID: 84885159085     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228296     Document Type: Article

References (59)

1. Goyenvalle, A., Seto, J. T., Davies, K. E., and Chamberlain, J. (2011) Therapeutic approaches to muscular dystrophy. Hum. Mol. Genet. 20, R69-78
2. Ryder-Cook, A. S., Sicinski, P., Thomas, K., Davies, K. E., Barnard, E. A, Darlison, M. G., and Barnard, P. J. (1988) Localization of the mdx mutation within the mouse dystrophin gene. EMBOJ. 7, 3017-3021
3. Petrof, B. J., Shrager, J. B., Stedman, H. H., Kelly, A. M., and Sweeney, H. L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. U. S. A. 90, 3710-3714
4. Grounds, M. D., Radley, H. G, Lynch, G. S., Nagaraju, K., and De Luca, A. (2008) Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis. 31, 1-19
5. Tinsley, J. M., Fairclough, R. J., Storer, R, Wilkes, F. J., Potter, A. C, Squire, S. E., Cozzoli, A, Capogrosso, R. F., Lambert, A, Wilson, F. X., Wren, S. P., De Luca, A, and Davies, K. E. (2011) Daily treatment with SMTC 1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS One 6, e19189
6. Collins, C. A, Olsen, I., Zammit, P. S., Heslop, L., Petrie, A, Partridge, T. A, and Morgan, J. E. (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289-301
7. Ljubicic, V., Miura, P., Burt, M., Boudreault, L., Lunde, J. A, Renaud, J. M., and Jasmin, B. J. (2011) Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum. Mol. Genet. 20, 3478-3493
8. Pauly, M., Daussin, F., Burelle, Y., Li, T., Koechlin-Ramonatxo, C, Hugon, G, Lacampagne, A, Coisy-Quivy, M., Liang, F., Hussain, S., Matecki, S., and Petrof, B. J. (2012) AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am. J. Pathol. 181, 583-592
9. Handschin, C, Kobayashi, Y. M., Chin, S., Seale, P., Campbell, K. P., and Spiegelman, B. M. (2007) PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev. 21, 770-783
10. Selsby, J. T., Morine, K. J., Pendrak, K., Barton, E. R, and Sweeney, H. L. (2012) Rescue of dystrophic skeletal muscle by PGC-1alpha involves a fast to slow fiber type shift in the mdx mouse. PLoS One 7, e30063
11. Jahnke, V. E., Van der Meulen, J. H., Johnston, H. K., Ghimbovschi, S., Hoffman, E. P., and Nagaraju, K (2012) Metabolic remodeling agents show beneficial effects in the dystrophin-deficient mdx mouse model. Skelet. Muscle 2, 16
12. Miura, P., Chakkalakal, J. V., Boudreault, L., Belanger, G, Hebert, R. L., and Jasmin, B. J. (2009) Pharmacological activation of PPARbeta/delta stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum. Mol. Genet. 18, 4640-4649
13. Deasy, B. M., Feduska, J. M., Payne, T. R., Li, Y., and Huard, J. (2009) Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. Mol. Ther. 17, 1788-1798
14. Messina, S., Mazzeo, A., Bitto, A., Aguennouz, M., De Pasquale, M. G., Minutoli, L., Altavilla, D., Zentilin, L., Giacca, M., Squadrito, F., and Vita, G. (2007) VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J. 21, 3737-3746
15. Neuhaus, P., Oustanina, S., Loch, T., Kruger, M., Dono, R., Zeller, R., and Braun, T. (2003) Reduced mobility of fibroblast growth factor (FGF)-deficient myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple-mutant mice. Mol. Cell. Biol. 23, 6037-6048
16. Giguere, V. (2008) Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev. 29, 677-696
17. Heard, D. J., Norby, P. L., Holloway, J., and Vissing, H. (2000) Human ERRgamma, a third member of the estrogen receptorrelated receptor (ERR) subfamily of orphan nuclear receptors: tissue-specific isoforms are expressed during development and in the adult. Mol. Endocrinol. 14, 382-392
18. Hong, H., Yang, L., and Stallcup, M. R. (1999) Hormoneindependent transcriptional activation and coactivator binding by novel orphan nuclear receptor ERR3. J. Biol. Chem. 274, 22618-22626
19. Wang, S. C., Myers, S., Dooms, C., Capon, R., and Muscat, G. E. (2010) An ERRbeta/gamma agonist modulates GRalpha expression, and glucocorticoid responsive gene expression in skeletal muscle cells. Mol. Cell. Endocrinol. 315, 146-152
20. Narkar, V. A., Fan, W., Downes, M., Yu, R. T., Alaynick, W. A., Banayo, E., Karunasiri, M. S., Lorca, S., and Evans, R. M. (2011) Exercise and PGC-1alpha-independent synchronization of type I muscle metabolism and vasculature by ERRgamma. Cell Metab. 13, 283-293
21. Matsakas, A., Yadav, V., Lorca, S., Evans, R. M., and Narkar, V. A. (2012) Revascularization of ischemic skeletal muscle by estrogen-related receptor-gamma. Circ. Res. 110, 1087-1096
22. Matsakas, A., Macharia, R., Otto, A., Elashry, M. I., Romanello, V., Sartori, R., Amthor, H., Sandri, M., Narkar, V., and Patel, K. (2012) Exercise training attenuates the hypermuscular phenotype and restores skeletal muscle function in the myostatin null mouse. Exp. Physiol. 97, 125-140
23. Matsakas, A., Mouisel, E., Amthor, H., and Patel, K. (2010) Myostatin knockout mice increase oxidative muscle phenotype as an adaptive response to exercise. J. Muscle Res. Cell Motil. 31, 111-125
24. Kobayashi, Y. M., Rader, E. P., Crawford, R. W., Iyengar, N. K., Faulkner, J. A., Parikh, S. V., Weiss, R. M., Chamberlain, J. S., Moore, S. A., and Campbell, K. P. (2008) Sarcolemma-localized nNOS is required to maintain activity after mild exercise. Nature 456, 511-515
25. Thomas, G. D., Sander, M., Lau, K. S., Huang, P. L., and Victor, R. G. (1998) Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 95, 15090-15095
26. Sander, M., Chavoshan, B., Harris, S. A., Iannaccone, S. T., Thomas, G. D., and Victor, R. G. (2000) Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U. S. A. 97, 13818-13823
27. Deconinck, N., Tinsley, J., De Backer, F., Fisher, R., Phelps, S., Davies, K., and Gillis, J. M. (1997) Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat. Med. 3, 1216-1221
28. Li, S., Kimura, E., Ng, R., Fall, B. M., Reyes, M., Faulkner, J. A., and Chamberlain, J. S. (2006) A highly functional mini-dystrophin/GFP fusion gene for cell and gene therapy studies of Duchenne muscular dystrophy. Hum. Mol. Genet. 15, 1610-1622
29. Phelps, S. F., Hauser, M. A., Cole, N. M., Rafael, J. A., Faulkner, J. A., and Chamberlain, J. S. (1995) Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4, 1251-1258
30. Rafael, J. A., Sunada, Y., Cole, N. M., Campbell, K. P., and Chamberlain, J. S. (1994) Prevention of dystrophic pathology in mdx mice by a truncated dystrophin isoform. Hum. Mol. Genet. 3, 1725-1733
31. Rafael, J. A., Tinsley, J. M., Potter, A. C., Deconinck, A. E., and Davies, K. E. (1998) Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat. Genet. 19, 79-82
32. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Gillis, J. M., and Davies, K. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med. 4, 1441-1444
33. Tinsley, J. M., Potter, A. C., Phelps, S. R., Fisher, R., and Davies, K. E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384, 349-353
34. Chakkalakal, J. V., Stocksley, M. A., Harrison, M. A., Angus, L. M., St-Pierre, S., Megeney, L. A., Chin, E. R., Michel, R. N., and Jasmin, B. J. (2003) Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc. Natl. Acad. Sci. U. S. A. 100, 7791-7796
35. Gramolini, A. O., Belanger, G., Thompson, J. M., Chakkalakal, J. V., and Jasmin, B. J. (2001) Increased expression of utrophin in a slow vs.a fast muscle involves posttranscriptional events. Am. J. Physiol. Cell Physiol. 281, C1300-C1309
36. Chakkalakal, J. V., Harrison, M. A., Carbonetto, S., Chin, E., and Jasmin, B. J. (2004) Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum. Mol. Genet. 13, 379-388
37. Porter, J. D., Rafael, J. A., Ragusa, R. J., Brueckner, J. K., and Davies, K. E. (1998) The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J. Cell Sci. 111, 1801-1811
38. Khairallah, R. J., Shi, G., Sbrana, F., Prosser, B. L., Mazaitis, M. J., Hoffman, E. P., Mahurkar, A., Sachs, F., Sun, Y., Chen, Y. W., Raiteri, R., Lederer, W. J., Dorsey, S. G., and Ward, C. W. (2012) Microtubules underlie dysfunction in duchenne muscular dystrophy. Sci. Signal. 5, ra56
39. Robert, V., Massimino, M. L., Tosello, V., Marsault, R., Sorrentino, V., and Pozzan, T. (2001) Alteration in calcium handling at the subcellular level in mdx myotubes. J. Biol. Chem. 276, 4647-4651
40. Kuznetsov, A. V., Winkler, K., Wiedemann, F. R., Von Bossanyi, P., and Kunz, W. S. (1998) Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol. Cell. Biochem. 183, 87-96
41. Percival, J. M., Siegel, M. P., Knowels, G., and Marcinek, D. J. (2012) Defects in mitochondrial localization and ATP synthesis in the mdx mouse model of Duchenne muscular dystrophy are not alleviated by PDE5 inhibition. Hum. Mol. Genet. 22, 153-167
42. Alaynick, W. A., Kondo, R. P., Xie, W., He, W., Downes, M., Jonker, J. W., Giles, W., Naviaux, R. K., Giguere, V., and Evans, R. M. (2007) ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab. 6, 13-24
43. Dufour, C. R., Wilson, B. J., Huss, J. M., Kelly, D. P., Downes, M., Evans, R. M., Blanchette, M., and Giguere, V. (2007) Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and gamma. Cell Metab. 5, 345-356
44. Huss, J. M., Torra, I. P., Staels, B., Giguere, V., and Kelly, D. P. (2004) Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24, 9079-9091
45. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N., Willy, P. J., Schulman, I. G., Heyman, R. A., Lander, E. S., and Spiegelman, B. M. (2004) Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U. S. A. 101, 6570-6575
46. Rangwala, S. M., Wang, X., Calvo, J. A., Lindsley, L., Deyneko, G., Beaulieu, V., Gao, J., Turner, G., and Markovits, J. (2010) Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J. Biol. Chem. 285, 22619-22629
47. Arany, Z., Foo, S. Y., Ma, Y., Ruas, J. L., Girnun, G., Cooper, M., Laznik, D., Chinsomboon, J., Rangwala, S. M., Baek, K. H., Rosenzweig, A., and Spiegelman, B. M. (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451, 1008-1012
48. Chinsomboon, J., Ruas, J., Gupta, R. K., Thom, R., Rowe, G. C., Sawada, N., Raghuram, S., and Arany, Z. (2009) The transcriptional coactivator PGC-1alpha mediates exerciseinduced angiogenesis in skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 106, 21401-21406
49. Jager, S., Handschin, C., St-Pierre, J., and Spiegelman, B. M. (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 104, 12017-12022
50. Narkar, V. A., Downes, M., Yu, R. T., Embler, E., Banayo, E., Mihaylova, M. M., Nelson, M. C., Zou, Y., Juguilon, H., Kang, H., Shaw, R. J., and Evans, R. M. (2008) AMPK and PPARdelta agonists are exercise mimetics. Cell 134, 405-415
51. Shiao, T., Fond, A., Deng, B., Wehling-Henricks, M., Froehner, S. C., and Tidball, J. G. (2004) Defects in neuromuscular junction structure in dystrophic muscle are corrected by expression of a NOS transgene in dystrophindeficient muscles, but not in muscles lacking alpha-and beta1-syntrophins. Hum. Mol. Genet. 13, 1873-1884
52. Tidball, J. G., and Wehling-Henricks, M. (2004) Expression of a NOS transgene in dystrophin-deficient muscle reduces muscle membrane damage without increasing the expression of membrane-associated cytoskeletal proteins. Mol. Genet. Metab. 82, 312-320
53. Wehling, M., Spencer, M. J., and Tidball, J. G. (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 155, 123-131
54. Borselli, C., Storrie, H., Benesch-Lee, F., Shvartsman, D., Lichtman, J. W., Vandenburgh, H. H., and Mooney, D. J. (2010) Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc. Natl. Acad. Sci. U. S. A. 107, 3287-3292
55. Murray, J., Auwerx, J., and Huss, J. M. (2012) Impaired myogenesis in estrogen-related receptor gamma (ERRgamma)-deficient skeletal myocytes due to oxidative stress. FASEB J. 27, 135-150
56. Faist, V., Konig, J., Hoger, H., and Elmadfa, I. (2001) Decreased mitochondrial oxygen consumption and antioxidant enzyme activities in skeletal muscle of dystrophic mice after low-intensity exercise. Ann. Nutr. Metab. 45, 58-66
57. Chakkalakal, J. V., Thompson, J., Parks, R. J., and Jasmin, B. J. (2005) Molecular, cellular, and pharmacological therapies for Duchenne/Becker muscular dystrophies. FASEB J. 19, 880-891
58. Fairclough, R. J., Bareja, A., and Davies, K. E. (2011) Progress in therapy for Duchenne muscular dystrophy. Exp. Physiol. 96, 1101-1113
59. Khurana, T. S., and Davies, K. E. (2003) Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug Discov. 2, 379-390