Utrophin A is essential in mediating the functional adaptations of mdx mouse muscle following chronic AMPK activation

Human Molecular Genetics

Volumn 24, Issue 5, 2015, Pages 1243-1255

  Al Rewashdy, Hasanen ^a   Ljubicic, Vladimir ^a   Lin, Wei ^a   Renaud, Jean Marc ^a   Jasmin, Bernard J ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN M; MOLECULAR MARKER; MUSCLE PROTEIN; UNCLASSIFIED DRUG; UTROPHIN; UTROPHIN A; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; DYSTROGLYCAN; RIBONUCLEOSIDE; UTRN PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECCENTRIC MUSCLE CONTRACTION; ENZYME ACTIVATION; FEMALE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MORPHOLOGY; GENE EXPRESSION; GENE INACTIVATION; GENETIC ASSOCIATION; GRIP STRENGTH; KNOCKOUT MOUSE; MALE; MORPHOLOGICAL ADAPTATION; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE STRENGTH; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; SARCOLEMMA; SARCOPLASM; SIGNAL TRANSDUCTION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; GENETICS; GENOTYPING TECHNIQUE; HAND STRENGTH; METABOLISM; MUSCLE FIBRIL; PHYSIOLOGY;

ANIMALIA; MUS;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; FEMALE; GENOTYPING TECHNIQUES; HAND STRENGTH; MALE; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCULAR DYSTROPHY, DUCHENNE; MYOFIBRILS; PHENOTYPE; RIBONUCLEOSIDES; UTROPHIN;

EID: 84924455400     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu535     Document Type: Article

References (74)

1. Blake, D.J., Wier, A., Newey, S.E. and Davies, K.E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev., 82, 291-329.
2. Rando, T.A. (2001) The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve, 24, 1575-1594.
3. Amann, K.J., Guo, A.W. and Ervasti, J.M. (1999) Utrophin A lacks the rod domain actin binding activity of dystrophin. J. Biol. Chem., 274, 35375-35380.
4. Rybakova, I.N., Patel, J.R. and Ervasti, J.M. (2000) The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell Biol., 150, 1209-1214.
5. Ahn, A.H. and Kunkel, L.M. (1993) The structural and functional diversity of dystrophin. Nat. Genet., 3, 283-291.
6. Winder, S.J. (1997) The membrane-cytoskeleton interface: the role of dystrophin and utrophin A. J. Muscle Res. Cell Motil., 18, 617-629.
7. Koenig, M. and Kunkel, L.M. (1990) Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J. Biol. Chem., 265, 4560-4566.
8. 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. USA, 90, 3710-3714.
9. Morrison, J., Lu, Q.L., Pastoret, C., Partridge, T. and Bou-Gharios, G. (2000) T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab. Invest., 80, 881-891.
10. Bushby, K., Finkel, R., Birnkrant, D.J., Case, L.E., Clemens, P.R., Cripe, L., Kaul, A., Kinnett, K., McDonald, C., Pandya, S. et al. (2010) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol., 9, 77-93.
11. Bushby, K., Finkel, R., Birnkrant, D.J., Case, L.E., Clemens, P.R., Cripe, L., Kaul, A., Kinnett, K., McDonald, C., Pandya, S. et al. (2010) Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care. Lancet Neurol., 9, 177-189.
12. Pichavant, C., Aartsma-Rus, A., Clemens, P.R., Davies, K.E., Dickson, G., Takeda, S., Wilton, S.D., Wolff, J.A., Wooddell, C.I., Xiao, X. et al. (2011) Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol. Ther., 19, 830-840.
13. Webster, C., Silberstein, L., Hay, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
14. Moens, P., Baatsen, P.H. and Maréchal, G. (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J. Muscle Res. Cell Motil., 14, 446-451.
15. Love, D.R., Hill, D.F., Dickson, G., Spurr, N.K., Byth, B.C., Marsden, R.F., Walsh, F.S., Edwards, Y.H. and Davies, K.E. (1989) An autosomal transcript in skeletal muscle with homology to dystrophin. Nature, 339, 55-58.
16. Tinsley, J.M., Blake, D.J., Roche, A., Fairbrother, U., Riss, J., Byth, B.C., Knight, A.E., Kendrick Jones, J., Suthers, G.K., Love, D.R., Edwards, Y.H. and Davies, K.E. (1992) Primary structure of dystrophin-related protein. Nature, 360, 591-593.
17. Li, D., Bareja, A., Judge, L., Yue, Y., Lai, Y., Fairclough, R., Davies, K.E., Chamberlain, J.S. and Duan, D. (2010) Sarcolemmal nNOS anchoring reveals a qualitative difference between dystrophin and utrophin. J. Cell. Sci., 15, 2008-2013.
18. Belanto, J.J., Mader, T.L., Eckhoff, M.D., Strandjord, D.M., Banks, G.B., Gardner, M.K., Lowe, D.A. and Ervasti, J.M. (2014) Microtubule binding distinguishes dystrophin from utrophin. Proc. Natl. Acad. Sci. USA, 111, 5723-5728.
19. Squire, S., Raymackers, J.M., Vandebrouck, C., Potter, A., Tinsley, J., Fisher, R., Gillis, J.M. and Davies, K.E. (2002) Prevention of pathology in mdx mice by expression of utrophin A: analysis using an inducible transgenic expression system. Hum. Mol. Genet., 11, 3333-3344.
20. Krag, T.O., Bogdanovich, S., Jensen, C.J., Fischer, M.D., Hansen-Schwartz, J., Javazon, E.H., Flake, A.W., Edvinsson, L. and Khurana, T.S. (2004) Heregulin ameliorates the dystrophic phenotype in mdx mice. Proc. Natl Acad. Sci. USA, 101, 13856-13860.
21. Rafael, J.A., Tinsley, J.M., Potter, A.C., Deconinck, A.E. and Davies, K.E. (1998) Skeletal muscle-specific expression of a utrophin A transgene rescues utrophin A-dystrophin deficient mice. Nat. Genet., 19, 79-82.
22. Khurana, T.S.,Watkins, S.C., Chafey, P., Chelly, J., Tomé, F.M., Fardeau, M., Kaplan, J.C. and Kunkel, L.M. (1991) Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul. Disord., 1, 185-194.
23. Ohlendieck, K., Ervasti, J.M., Matsumura, K., Kahl, S.D., Leveille, C.J. and Campbell, K.P. (1991) Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron, 7, 499-508.
24. Gramolini, A.O., Bélanger, G., Thompson, J.M., Chakkalakal, J. V. and Jasmin, B.J. (2001) Increased expression of utrophin A in a slow versus a fast muscle involves posttranscriptional events. Am. J. Physiol. Cell Physiol., 281, C1300-C1309.
25. Angus, L.M., Chakkalakal, J.V., Méjat, A., Eibl, J.K., Bélanger, G., Megeney, L.A., Chin, E.R., Schaeffer, L., Michel, R.N. and Jasmin, B.J. (2005) Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1alpha, drives utrophin A gene expression at the neuromuscular junction. Am. J. Physiol. Cell Physiol., 289, C908-C917.
26. Chakkalakal, J.V., Harrison, M.A., Carbonetto, S., Chin, E., Michel, R.N. and Jasmin, B.J. (2004) Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum. Mol. Genet., 13, 379-388.
27. Chakkalakal, J.V., Michel, S., Chin, E.R., Michel, R.N. and Jasmin, B.J. (2006) Targeted inhibition of Ca2+/calmodulin signaling exacerbates the dystrophic phenotype in mdx mouse muscle. Hum. Mol. Genet., 15, 1423-1435.
28. Chakkalakal, J.V., Stocksley, M.A., Harrison, M.A., Angus, L.M., Deschenes-Furry, J., 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. USA, 100, 7791-7796.
29. Chakkalakal, J.V., Miura, P., Bélanger, G., Michel, R.N. and Jasmin, B.J. (2008) Modulation of utrophin A mRNA stability in fast versus slow muscles via an AU-rich element and calcineurin signaling. Nucleic Acids Res., 36, 826-838.
30. Webster, C., Silberstein, L., Hays, P. and Blau, M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
31. Ljubicic, V., Miura, P., Burt, M., Boudreault, L., Khogali, S., 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.
32. Ljubicic, V. and Jasmin, B.J. (2013) AMP-activated protein kinase at the nexus of therapeutic skeletal muscle plasticity in Duchenne muscular dystrophy. Trends Mol. Med., 19, 614-624.
33. Ljubicic, V., Khogali, S., Renaud, J.M. and Jasmin, B.J. (2012) Chronic AMPK stimulation attenuates adaptive signaling in dystrophic skeletal muscle. Am. J. Physiol. Cell Physiol., 302, C110-C121.
34. Miura, P., Chakkalakal, J.V., Boudreault, L., Bélanger, G., Hébert, R.L., Renaud, J.M. 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.
35. Baltgalvis, K.A., Call, J.A., Cochrane, G.D., Laker, R.C., Yan, Z. and Lowe, D.A. (2012) Exercise training improves plantarflexor muscle function in mdx mice. Med. Sci. Sports Exerc., 44, 1671-1679.
36. Blanchet, E., Annicotte, J.S., Pradelli, L.A., Hugon, G., Matecki, S., Mornet, D., Rivier, F. and Fajas, L. (2012) E2F transcription factor-1 deficiency reduces pathophysiology in the mouse model of Duchenne muscular dystrophy through increased muscle oxidative metabolism. Hum. Mol. Genet., 21, 3910-3917.
37. Bueno Júnior, C.R., Pantaleão, L.C., Voltarelli, V.A., Bozi, L.H., Brum, P.C. and Zatz, M. (2012) Combined effect of AMPK/ PPAR agonists and exercise training in mdx mice functional performance. PLoS One, 7, e45699.
38. Godin, R., Daussin, F.,Matecki, S., Li, T., Petrof, B.J. and Burelle, Y. (2012) Peroxisome proliferator-activated receptor γ coactivator1-α gene transfer restores mitochondrial biomass and improves mitochondrial calcium handling in post-necrotic mdx mouse skeletal muscle. J. Phsyiol., 590, 5487-5502.
39. Gordon, B.S., Delgado, D.C. and Kostek, M.C. (2013) Resveratrol decreases inflammation and increases utrophin A gene expression in the mdx mouse model of Duchenne muscular dystrophy. Clin. Nutr., 32, 104-111.
40. 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.
41. Jahnke, V.E., van der Meulen, J.H., Johnston, H.K., Ghimbovschi, S., Partridge, T., Hoffman, E.P. and Nagaraju, K. (2012) Metabolic remodeling agents show beneficial effects in the dystrophin-deficient mdx mouse model. Skelet. Muscle, 2, 16.
42. Matsakas, A., Yadav, V., Lorca, S. and Narkar, V. (2013) Muscle ERRγ mitigates Duchenne muscular dystrophy via metabolic and angiogenic reprogramming. FASEB J., 27, 4004-4016.
43. Selsby, J.T., Morine, K.J., Pendrak, K., Barton, E.R. and Sweeney, H.L. (2012) Rescue of dystrophic skeletal muscle by PGC-1α involves a fast to slow fiber type shift in the mdx mouse. PLoS One, 7, e30063.
44. Stupka, N., Plant, D.R., Schertzer, J.D., Emerson, T.M., Bassel-Duby, R., Olson, E.N. and Lynch, G.S. (2006) Activated calcineurin ameliorates contraction-induced injury to skeletal muscles of mdx dystrophic mice. J. Physiol., 575, 645-656.
45. Von Maltzahn, J., Renaud, J.M., Parise, G. and Rudnicki, M.A. (2012) Wnt7a treatment ameliorates muscular dystrophy. Proc. Natl. Acad. Sci. USA, 109, 20614-20619.
46. Ljubicic, V., Burt, M. and Jasmin, B. (2014) The therapeutic potential of skeletal muscle plasticity in Duchenne muscular dystrophy: phenotypic modifiers as pharmacologic targets. FASEB J., 28, 548-568.
47. Zhang, L., Frederich, M., He, H. and Balschi, J. (2006) Relationship between 5-aminoimidazole-4-carboxamide-ribotide and AMP-activated protein kinase activity in the perfused mouse heart. Am. J. Physiol. Heart Circ. Physiol., 290, H1235-H1243.
48. Pauly, M., Daussin, F., Burelle, Y., Li, T., Godin, R., Fauconnier, J., Koechlin-Ramonatxo, C., Hugon, G., Lacampagne, A., Coisy-Quivy, M. et al. (2012) AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am. J. Pathol., 181, 583-592.
49. Winder, W.W., Holmes, B.F., Rubink, D.S., Jensen, E.B., Chen, M. and Holloszy, J.O. (2000) Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol., 88, 2219-2226.
50. Fillmore, N., Jacobs, D.L., Mills, D.B., Winder, W.W. and Hancock, C.R. (2010) Chronic AMP-activated protein kinase activation and a high-fat diet have an additive effect on mitochondria in rat skeletal muscle. J. Appl. Physiol., 109, 511-520.
51. Bergeron, R., Ren, J.M., Cadman, K.S., Moore, I.K., Perret, P., Pypaert, M., Young, L.H., Semenkovich, C.F. and Shulman, G.I. (2001) Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol. Endocrinol. Metab., 281, E1340-E1346.
52. Steinberg, G.R., O'Neill, H.M., Dzamko, N.L., Galic, S., Naim, T., Koopman, R., Jørgensen, S.B., Honeyman, J., Hewitt, K., Chen, Z.P. et al. (2010) Whole body deletion of AMP-activated protein kinase β2 reduces muscle AMPK activity and exercise capacity. J. Biol. Chem., 28, 37198-37209.
53. Zong, H., Ren, J.M., Young, L.H., Pypaert, M., Mu, J., Birnbaum, M.J. and Shulman, G.I. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl Acad. Sci. USA, 99, 15983-15987.
54. Hood, D.A. (2001) Invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol., 90, 1137-1157.
55. Quinn, J.L., Huynh, T., Uaesoontrachoon, K., Tatem, K., Phadke, A., Van der Meulen, J.H., Yu, Q. and Nagaraju, K. (2013) Effects of dantrolene therapy on disease phenotype in dystrophin deficient mdx mice. PLoS Curr., 1, 1-14.
56. Ljubicic, V., Burt,M., Lunde, J.A. and Jasmin, B.J. (2014) Resveratrol induces expression of the slow, oxidative phenotype inmdx mouse muscle together with enhanced activity of the SIRT1-PGC-1α axis. Am. J. Physiol. Cell Physiol. [Epub. ahead of prints].
57. Long, Y.C. and Zierath, J.R. (2008) Influence of AMP-activated protein kinase and calcineurin on metabolic networks in skeletal muscle. Am. J. Physiol. Endocrinol. Metab., 295, E545-E552.
58. Stupka, N., Gregorevic, P., Plant, D.R. and Lynch, G.S. (2004) The calcineurin signal transduction pathway is essential for successful muscle regeneration in mdx dystrophic mice. Acta. Neuropathol., 107, 299-310.
59. Straub, V., Rafael, J.A., Chamberlain, J.S. and Campbell, K.P. (1997) Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol., 139, 375-385.
60. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J.M. and Davies, K. (1998) Expression of full-length utrophin A prevents muscular dystrophy in mdx mice. Nat. Med., 4, 1441-1444. H1243.
61. Buetler, T.M., Renard, M., Offord, E.A., Schneider, H. and Ruegg, U.T. (2002) Green tea extract decreases muscle necrosis in mdx mice and protects against reactive oxygen species. Am. J. Clin. Nutr., 75, 749-753.
62. Call, J.A., Voelker, K.A.,Wolff, A.V., Mcmillan, R.P., Evans, N.P., Hulver, M.W., Talmadge, R.J. and Grange, R.W. (2008) Endurance capacity in maturing mdx mice is markedly enhanced by combined voluntary wheel running and green tea extract. J. Appl. Physiol., 105, 923-932.
63. Nakae, Y., Dorchies, O.M., Stoward, P.J., Zimmermann, B.F., Ritter, C. and Ruegg, U.T. (2012) Quantitative evaluation of the beneficial effects in the mdx mouse of epigallocatechin gallate, an antioxidant polyphenol from green tea. Histochem. Cell Biol., 137, 811-827.
64. Katsetos, S., Koutzaki, S. and Melvin, J. (2013) Mitochondrial dysfunction in neuromuscular disorders. Semin Pediatr Neurol., 20, 202-215.
65. Adhihetty, P.J., O'Leary, M.F. and Hood, D.A. (2008) Mitochondria in skeletal muscle: adaptable rheostats of apoptotic susceptibility. Exerc. Sport Sci. Rev., 36, 116-121.
66. Pagel-Langenickel, I., Bao, J., Pang, L. and Sack, M.N. (2010) The role of mitochondria in the pathophysiology of skeletal muscle insulin resistance. Endocr. Rev., 31, 25-51.
67. Millay, D.P., Sargent, M.A., Osinska, H., Baines, C.P., Barton, E. R., Vuagniaux, G., Sweeney, H.L., Robbins, J. and Molkentin, J. D. (2008) Genetic and pharmacologic inhibition of mitochondrial- dependent necrosis attenuates muscular dystrophy. Nat. Med., 14, 442-447.
68. Menazza, S., Blaauw, B., Tiepolo, T., Toniolo, L., Braghetta, P., Spolaore, B., Reggiani, C., Di Lisa, F., Bonaldo, P. and Canton, M. (2010) Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum. Mol. Genet., 19, 4207-4215.
69. Chan, M.C., Rowe, G.C., Raghuram, S., Patten, I.S., Farrell, C. and Arany, Z. (2014) Post-natal induction of PGC-1α protects against severe muscle dystrophy independently of utrophin A. Skelet. Muscle., 4, 2.
70. Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Puigserver, P., Isotani, E., Olson, E.N. et al. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature, 418, 797-801.
71. Schiaffino, S., Sandri, M. and Murgia, M. (2007) Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology, 22, 269-278.
72. Merrick, D., Stadler, L.K., Larner, D. and Smith, J. (2009) Muscular dystrophy begins early in embryonic development deriving from stem cell loss and disrupted skeletal muscle formation. Dis. Model Mech., 4, 374-388.
73. Pold, R., Jensen, L.S., Jessen, N., Buhl, E.S., Schmitz, O., Flyvbjerg, A., Fujii, N., Goodyear, L.J., Gotfredsen, C.F., Brand, C.L. et al. (2005) Long-term AICAR administration and exercise prevents diabetes in ZDF rats. Diabetes, 54, 928-934.
74. Buhl, E.S., Jessen, N., Pold, R., Ledet, T., Flyvbjerg, A., Pedersen, S.B., Pedersen, O., Schmitz, O. and Lund, S. (2002) Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes, 51, 2199-2206.