Rescue of dystrophic skeletal muscle by PGC-1α involves restored expression of dystrophin-associated protein complex components and satellite cell signaling

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 1, 2013, Pages

  Hollinger, Katrin ^a   Gardan Salmon, Delphine ^a   Santana, Connie ^a   Rice, Drance ^a   Snella, Elizabeth ^a   Selsby, Joshua T ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Duchenne muscular dystrophy; Gene expression; Mdx; Oxidative; Utrophin

Indexed keywords

DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; GENE TRANSFER; HINDLIMB; MOUSE; MUSCLE INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE SATELLITE CELL;

DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION; MDX; OXIDATIVE; UTROPHIN;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DYSTROPHIN; DYSTROPHIN-ASSOCIATED PROTEIN COMPLEX; GENETIC THERAPY; MICE; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; UP-REGULATION; UTROPHIN;

EID: 84879418084     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00221.2012     Document Type: Article

References (67)

1. Amenta AR, Yilmaz A, Bogdanovich S, McKechnie BA, Abedi M, Khurana TS, Fallon JR. Biglycan recruits utrophin to the sarcolemma and counters dystrophic pathology in mdx mice. Proc Natl Acad Sci USA 108: 762-767, 2011.
2. Angus LM, Chakkalakal JV, Mejat A, Eibl JK, Belanger G, Megeney LA, Chin ER, Schaeffer L, Michel RN, Jasmin BJ. Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1α, drives utrophin gene expression at the neuromuscular junction. Am J Physiol Cell Physiol 289: C908-C917, 2005.
3. Barton ER. Restoration of gamma-sarcoglycan localization and mechanical signal transduction are independent in murine skeletal muscle. J Biol Chem 285: 17263-17270, 2010.
4. Barton ER, Wang BJ, Brisson BK, Sweeney HL. Diaphragm displays early and progressive functional deficits in dysferlin-deficient mice. Muscle Nerve 42: 22-29, 2010.
5. Bertoni C. Clinical approaches in the treatment of Duchenne muscular dystrophy (DMD) using oligonucleotides. Front Biosci 13: 517-527, 2008.
6. Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP. Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromusc Disord 14: 675-682, 2004.
7. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192, 1984.
8. Byers TJ, Kunkel LM, Watkins SC. The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J Cell Biol 115: 411-421, 1991.
9. Chamberlain JS, Metzger J, Reyes M, Townsend D, Faulkner JA. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J 21: 2195-2204, 2007.
10. Christie KN. Chymostatin has no apparent beneficial effect on muscular dystrophy in the mdx mouse. J Neurol Sci 84: 341-346, 1988.
11. Corrado K, Mills PL, Chamberlain JS. Deletion analysis of the dystrophin-actin binding domain. FEBS Lett 344: 255-260, 1994.
12. De Palma C, Morisi F, Cheli S, Pambianco S, Cappello V, Vezzoli M, Rovere-Querini P, Moggio M, Ripolone M, Francolini M, Sandri M, Clementi E. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis 3: e418, 2012.
13. Disatnik MH, Dhawan J, Yu Y, Beal MF, Whirl MM, Franco AA, Rando TA. Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state. J Neurol Sci 161: 77-84, 1998.
14. Duance VC, Stephens HR, Dunn M, Bailey AJ, Dubowitz V. A role for collagen in the pathogenesis of muscular dystrophy? Nature 284: 470-472, 1980.
15. Emery AE. The muscular dystrophies. Lancet 359: 687-695, 2002.
16. Friedrichs M, Wirsdöerfer F, Flohé SB, Schneider S, Wuelling M, Vortkamp A. BMP signaling balances proliferation and differentiation of muscle satellite cell descendants. BMC Cell Biol 12: 26, 2011.
17. Gardan-Salmon D, Dixon JM, Lonergan SM, Selsby JT. Proteomic assessment of the acute phase of dystrophin deficiency in mdx mice. Eur J Appl Physiol 111: 2763-2773, 2011.
18. Godin R, Daussin F, Matecki S, Li T, Petrof BJ, Burelle Y. Peroxisome proliferator-activated receptor coactivator 1-gene transfer restores mitochondrial biomass and improves mitochondrial calcium handling in postnecrotic mdx mouse skeletal muscle. J Physiol 590: 5487-5502, 2012.
19. Gramolini AO, Belanger G, Thompson JM, Chakkalakal JV, Jasmin BJ. Increased expression of utrophin in a slow vs. a fast muscle involves posttranscriptional events. Am J Physiol Cell Physiol 281: C1300-C1309, 2001.
20. Gramolini AO, Dennis CL, Tinsley JM, Robertson GS, Cartaud J, Davies KE, Jasmin BJ. Local transcriptional control of utrophin expression at the neuromuscular synapse. J Biol Chem 272: 8117-8120, 1997.
21. Handschin C, Choi CS, Chin S, Kim S, Kawamori D, Kurpad AJ, Neubauer N, Hu J, Mootha VK, Kim YB, Kulkarni RN, Shulman GI, Spiegelman BM. Abnormal glucose homeostasis in skeletal musclespecific PGC-1α knockout mice reveals skeletal muscle-pancreatic β-cell crosstalk. J Clin Invest 117: 3463-3474, 2007.
22. Handschin C, Kobayashi YM, Chin S, Seale P, Campbell KP, Spiegelman BM. PGC-1α regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 21: 770-783, 2007.
23. Hirst RC, McCullagh KJ, Davies KE. Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol 24: 209-216, 2005.
24. Hori YS, Kuno A, Hosoda R, Tanno M, Miura T, Shimamoto K, Horio Y. Resveratrol ameliorates muscular pathology in the dystrophic mdx mouse, a model for Duchenne muscular dystrophy. J Pharmacol Exp Ther 338: 784-794, 2011.
25. Khurana TS, Watkins SC, Chafey P, Chelly J, Tome FM, Fardeau M, Kaplan JC, Kunkel LM. Immunolocalization and developmental expression of dystrophin-related protein in skeletal muscle. Neuromuscul Disord 1: 185-194, 1991.
26. Law DJ, Allen DL, Tidball JG. Talin, vinculin and DRP (utrophin) concentrations are increased at mdx myotendinous junctions following onset of necrosis. J Cell Sci 107: 1477-1483, 1994.
27. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106: 847-856, 2000.
28. Leick L, Wojtaszewski JF, Johansen ST, Kiilerich K, Comes G, Hellsten Y, Hidalgo J, Pilegaard H. PGC-1α is not mandatory for exercise-and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab 294: E463-E474, 2008.
29. Li D, Bareja A, Judge L, Yue Y, Lai Y, Fairclough R, Davies KE, Chamberlain JS, Duan D. Sarcolemmal nNOS anchoring reveals a qualitative difference between dystrophin and utrophin. J Cell Sci 123: 2008-2013, 2010.
30. 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. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002.
31. Ljubicic V, Miura P, Burt M, Boudreault L, Khogali S, Lunde JA, Renaud JM, Jasmin BJ. Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum Mol Genet 20: 3478-3493, 2011.
32. Lucas-Heron B, Schmitt N, Ollivier B. Muscular dystrophy: possible role of mitochondrial deficiency in muscle degeneration processes. J Neurol Sci 95: 327-334, 1990.
33. McGeachie JK, Grounds MD, Partridge TA, Morgan JE. Age-related changes in replication of myogenic cells in mdx mice: quantitative autoradiographic studies. J Neurol Sci 119: 169-179, 1993.
34. Miller G, Moore CJ, Terry R, La Riviere T, Mitchell A, Piggott R, Dear TN, Wells DJ, Winder SJ. Preventing phosphorylation of dystroglycan ameliorates the dystrophic phenotype in mdx mouse. Hum Mol Genet 21: 4508-4520, 2012.
35. Miura P, Chakkalakal JV, Boudreault L, Belanger G, Hebert RL, Renaud JM, Jasmin BJ. Pharmacological activation of PPARδ/ stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum Mol Genet 18: 4640-4649, 2009.
36. Moorwood C, Liu M, Tian Z, Barton ER. Isometric and eccentric force generation assessment of skeletal muscles isolated from murine models of muscular dystrophies. J Vis Exp e50036, 2013.
37. 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. Erralpha and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 101: 6570-6575, 2004.
38. Morine KJ, Bish LT, Selsby JT, Gazzara JA, Pendrak K, Sleeper MM, Barton ER, Lee SJ, Sweeney HL. Activin IIB receptor blockade attenuates dystrophic pathology in a mouse model of Duchenne muscular dystrophy. Muscle Nerve 42: 722-730, 2010.
39. Morris CA, Selsby JT, Morris LD, Pendrak K, Sweeney HL. Bowman-Birk inhibitor attenuates dystrophic pathology in mdx mice. J Appl Physiol 109: 1492-1499, 2010.
40. Nikolic N, Rhedin M, Rustan AC, Storlien L, Thoresen GH, Stromstedt M. Overexpression of PGC-1α increases fatty acid oxidative capacity of human skeletal muscle cells. Biochem Res Int 2012: 714074, 2012.
41. Odom GL, Gregorevic P, Allen JM, Finn E, Chamberlain JS. Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/utrophin-deficient mice. Mol Ther 16: 1539-1545, 2008.
42. Ono Y, Calhabeu F, Morgan JE, Katagiri T, Amthor H, Zammit PS. BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ 18: 222-234, 2011.
43. Pauly M, Daussin F, Burelle Y, Li T, Godin R, Fauconnier J, Koechlin-Ramonatxo C, Hugon G, Lacampagne A, Coisy-Quivy M, Liang F, Hussain S, Matecki S, Petrof BJ. AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 181: 583-592, 2012.
44. Pearce M, Blake DJ, Tinsley JM, Byth BC, Campbell L, Monaco AP, Davies KE. The utrophin and dystrophin genes share similarities in genomic structure. Hum Mol Genet 2: 1765-1772, 1993.
45. Radley HG, Grounds MD. Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice. Neurobiol Dis 23: 387-397, 2006.
46. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE. Skeletal muscle-specific expression of a utrophin transgene rescues utrophindystrophin deficient mice. Nat Genet 19: 79-82, 1998.
47. Rayavarapu S, Coley W, Cakir E, Jahnke V, Takeda S, Aoki Y, Gordish-Dressman H, Jaiswal JK, Hoffman EP, Brown KJ, Hathout Y, Nagaraju K. Identification of disease-specific pathways using in vivo SILAC proteomics in dystrophin-deficient mdx mouse. Mol Cell Proteomics 12: 1061-1073, 2013.
48. Ridgeway AG, Wilton S, Skerjanc IS. Myocyte enhancer factor 2C and myogenin up-regulate each other's expression and induce the development of skeletal muscle in P19 cells. J Biol Chem 275: 41-46, 2000.
49. Rybakova IN, Amann KJ, Ervasti JM. A new model for the interaction of dystrophin with F-actin. J Cell Biol 135: 661-672, 1996.
50. Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA. Reduced differentiation potential of primary MyoD-/-myogenic cells derived from adult skeletal muscle. J Cell Biol 144: 631-643, 1999.
51. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. PGC-1 alpha a protects skeletal muscle from atrophy by suppressing Fox03 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103: 16260-16265, 2006.
52. Selsby J, Morine K, Pendrak K, Barton E, Sweeney HL. Rescue of dystrophic skeletal muscle by PGC-1a involves a fast to slow fiber type shift in the mdx mouse. PLoS One 7: e30063, 2012.
53. Selsby J, Morris C, Morris L, Sweeney L. A proteasome inhibitor fails to attenuate dystrophic pathology in mdx mice. PLoS Currents 4: e4f84a944d8930, 2012.
54. Selsby J, Pendrak K, Zadel M, Tian Z, Pham J, Carver T, Acosta P, Barton E, Sweeney HL. Leupeptin-based inhibitors do not improve the mdx phenotype. Am J Physiol Regul Integr Comp Physiol 299: R1192-R1201, 2010.
55. Selsby JT. Increased catalase expression improves muscle function in mdx mice. Exp Physiol 96: 194-202, 2011.
56. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580, 1989.
57. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539, 1991.
58. Sterrenburg E, van der Wees CG, White SJ, Turk R, de Menezes RX, van Ommen GJ, den Dunnen JT, 't Hoen PA. Gene expression profiling highlights defective myogenesis in DMD patients and a possible role for bone morphogenetic protein 4. Neurobiol Dis 23: 228-236, 2006.
59. Summermatter S, Baum O, Santos G, Hoppeler H, Handschin C. Peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) promotes skeletal muscle lipid refueling in vivo by activating de novo lipogenesis and the pentose phosphate pathway. J Biol Chem 285: 32793-32800, 2010.
60. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4: 1441-1444, 1998.
61. Tinsley JM, Blake DJ, Roche A, Fairbrother U, Riss J, Byth BC, Knight AE, Kendrick-Jones J, Suthers GK, Love DR, Edwards YH, Davies, KE. Primary structure of dystrophin-related protein. Nature 360: 591-593, 1992.
62. Tinsley JM, Fairclough RJ, Storer R, Wilkes FJ, Potter AC, Squire SE, Powell DS, Cozzoli A, Capogrosso RF, Lambert A, Wilson FX, Wren SP, De Luca A, Davies KE. Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLos One 6: e19189, 2011.
63. Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, Davies KE. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384: 349-353, 1996.
64. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, Moraes CT. Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA 106: 20405-20410, 2009.
65. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.
66. Yablonka-Reuveni Z, Seger R, Rivera AJ. Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47: 23-42, 1999.
67. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR. Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119: 1824-1832, 2006.