Exercise increases utrophin protein expression in the mdx mouse model of Duchenne muscular dystrophy

Muscle and Nerve

Volumn 49, Issue 6, 2014, Pages 915-918

  Gordon, Bradley S ^a   Lowe, Dawn A ^b   Kostek, Matthew C ^c  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c DUQUESNE UNIVERSITY   (United States)

Author keywords

Dystrophin; Genetic disease; Skeletal muscle; Therapy; Treatment

Indexed keywords

UTROPHIN;

AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EXERCISE; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUADRICEPS FEMORIS MUSCLE; RUNNING; SITTING; SOLEUS MUSCLE;

DYSTROPHIN; GENETIC DISEASE; SKELETAL MUSCLE; THERAPY; TREATMENT;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; MALE; MICE; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PHYSICAL CONDITIONING, ANIMAL; RNA, MESSENGER; UTROPHIN;

EID: 84900520224     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.24151     Document Type: Article

References (40)

1. Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987;51:919-928.
2. Nelson SF, Crosbie RH, Miceli MC, Spencer MJ. Emerging genetic therapies to treat Duchenne muscular dystrophy. Curr Opin Neurol 2009;22:532-538.
3. Tidball JG, Wehling-Henricks M. Evolving therapeutic strategies for Duchenne muscular dystrophy: targeting downstream events. Pediatr Res 2004;56:831-841.
4. Campbell KP. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 1995;80:675-679.
5. Deconinck N, Dan B. Pathophysiology of duchenne muscular dystrophy: current hypotheses. Pediatr Neurol 2007;36:1-7.
6. Collins CA, Morgan JE. Duchenne's muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies. Int J Exp Pathol 2003;84:165-172.
7. Perkins KJ, Davies KE. The role of utrophin in the potential therapy of Duchenne muscular dystrophy. Neuromuscul Disord 2002;12(Suppl 1):S78-S89.
8. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, et al. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 1998;4:1441-1444.
9. Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D, Phelps S, et al. Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med 1997;3:1216-1221.
10. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE. Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 1998;19:79-82.
11. Squire S, Raymackers JM, Vandebrouck C, Potter A, Tinsley J, Fisher R, et al. Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum Mol Genet 2002;11:3333-3344.
12. Ahmad N, Welch I, Grange R, Hadway J, Dhanvantari S, Hill D, et al. Use of imaging biomarkers to assess perfusion and glucose metabolism in the skeletal muscle of dystrophic mice. BMC Musculoskelet Disord 2011;12:127.
13. De Luca A, Pierno S, Liantonio A, Cetrone M, Camerino C, Fraysse B, et al. Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J Pharmacol Exp Ther 2003;304:453-463.
14. Markert CD, Ambrosio F, Call JA, Grange RW. Exercise and Duchenne muscular dystrophy: toward evidence-based exercise prescription. Muscle Nerve 2011;43:464-478.
15. de Lateur BJ, Giaconi RM. Effect on maximal strength of submaximal exercise in Duchenne muscular dystrophy. Am J Phys Med 1979;58:26-36.
16. Vignos PJ Jr, Watkins MP. The effect of exercise in muscular dystrophy. JAMA 1966;197:843-848.
17. Jansen M, van Alfen N, Geurts AC, de Groot IJ. Assisted bicycle training delays functional deterioration in boys with Duchenne muscular dystrophy: the randomized controlled trial "no use is disuse". Neurorehabil Neural Repair 2013;27:816-827.
18. Call JA, McKeehen JN, Novotny SA, Lowe DA. Progressive resistance voluntary wheel running in the mdx mouse. Muscle Nerve 2010;42:871-880.
19. Call JA, Voelker KA, Wolff AV, McMillan RP, Evans NP, Hulver MW, et al. Endurance capacity in maturing mdx mice is markedly enhanced by combined voluntary wheel running and green tea extract. J Appl Physiol 2008;105:923-932.
20. Carter GT, Wineinger MA, Walsh SA, Horasek SJ, Abresch RT, Fowler WM, Jr. Effect of voluntary wheel-running exercise on muscles of the mdx mouse. Neuromuscul Disord 1995;5:323-332.
21. Dupont-Versteegden EE, McCarter RJ, Katz MS. Voluntary exercise decreases progression of muscular dystrophy in diaphragm of mdx mice. J Appl Physiol 1994;77:1736-1741.
22. Hayes A, Williams DA. Beneficial effects of voluntary wheel running on the properties of dystrophic mouse muscle. J Appl Physiol 1996;80:670-679.
23. Landisch RM, Kosir AM, Nelson SA, Baltgalvis KA, Lowe DA. Adaptive and nonadaptive responses to voluntary wheel running by mdx mice. Muscle Nerve 2008;38:1290-1303.
24. Timmons JA, Larsson O, Jansson E, Fischer H, Gustafsson T, Greenhaff PL, et al. Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy. FASEB J 2005;19:750-760.
25. Baltgalvis KA, Call JA, Cochrane GD, Laker RC, Yan Z, Lowe DA. Exercise training improves plantar flexor muscle function in mdx mice. Med Sci Sports Exerc 2012;44:1671-1679.
26. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, et al. Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 2001;20:6414-6423.
27. Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 2001;155:123-131.
28. Gordon BS, Delgado Diaz DC, Kostek MC. Resveratrol decreases inflammation and increases utrophin gene expression in the mdx mouse model of duchenne muscular dystrophy. Clin Nutr 2013;32:104-111.
29. Selsby JT, Acosta P, Sleeper MM, Barton ER, Sweeney HL. Long-term wheel running compromises diaphragm function but improves cardiac and plantarflexor function in the mdx mouse. J Appl Physiol (1985) 2013;115:660-666.
30. Radley HG, Davies MJ, Grounds MD. Reduced muscle necrosis and long-term benefits in dystrophic mdx mice after cV1q (blockade of TNF) treatment. Neuromuscul Disord 2008;18:227-238.
31. Partridge T. Animal models of muscular dystrophy--what can they teach us? Neuropathol Appl Neurobiol 1991;17:353-363.
32. Partridge TA. The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J 2013;280:4177-4186.
33. Miura P, Thompson J, Chakkalakal JV, Holcik M, Jasmin BJ. The utrophin A 5'-untranslated region confers internal ribosome entry site-mediated translational control during regeneration of skeletal muscle fibers. J Biol Chem 2005;280:32997-33005.
34. Miura P, Andrews M, Holcik M, Jasmin BJ. IRES-mediated translation of utrophin A is enhanced by glucocorticoid treatment in skeletal muscle cells. PloS One 2008;3:e2309.
35. Miura P, Coriati A, Belanger G, De Repentigny Y, Lee J, Kothary R, et al. The utrophin A 5'-UTR drives cap-independent translation exclusively in skeletal muscles of transgenic mice and interacts with eEF1A2. Hum Mol Genet 2010;19:1211-1220.
36. Williamson DL, Kubica N, Kimball SR, Jefferson LS. Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 2006;573:497-510.
37. Handschin C, Kobayashi YM, Chin S, Seale P, Campbell KP, Spiegelman BM. PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 2007;21:770-783.
38. Selsby JT, Morine KJ, Pendrak K, Barton ER, Sweeney HL. Rescue of dystrophic skeletal muscle by PGC-1alpha involves a fast to slow fiber type shift in the mdx mouse. PloS One 2012;7:e30063.
39. Chakkalakal JV, Stocksley MA, Harrison MA, Angus LM, Deschenes-Furry J, St-Pierre S, et al. 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 2003;100:7791-7796.
40. Rafael JA, Townsend ER, Squire SE, Potter AC, Chamberlain JS, Davies KE. Dystrophin and utrophin influence fiber type composition and post-synaptic membrane structure. Hum Mol Genet 2000;9:1357-1367.