Myogenic Akt signaling attenuates muscular degeneration, promotes myofiber regeneration and improves muscle function in dystrophin-deficient mdx mice

Human Molecular Genetics

Volumn 20, Issue 7, 2011, Pages 1324-1338

  Kim, Michelle H ^a   Kay, Danielle I ^a   Rudra, Renuka T ^a   Chen, Bo Ming ^a   Hsu, Nigel ^a   Izumiya, Yasuhiro ^a   Martinez, Leonel ^a   Spencer, Melissa J ^a   Walsh, Kenneth ^a   Grinnell, Alan D ^a   Crosbie, Rachelle H ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOTOXIN; DYSTROPHIN; PROTEIN KINASE B; SERUM ALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ENZYME ACTIVATION; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; GRIP STRENGTH; HISTOPATHOLOGY; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOLEMMA; SIGNAL TRANSDUCTION;

ANIMALS; DYSTROPHIN; HUMANS; MICE; MICE, INBRED MDX; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MUSCULAR DYSTROPHY, ANIMAL; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

MUS;

EID: 79952603226     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr015     Document Type: Article

References (69)

1. Hoffman, E.P., Brown, R.H. Jr. and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
2. Campbell, K.P. and Kahl, S.D. (1989) Association of dystrophin and an integral membrane glycoprotein. Nature, 338, 259-262.
3. Ervasti, J.M., Ohlendieck, K., Kahl, S.D., Gaver, M.G. and Campbell, K.P. (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature, 345, 315-319.
4. Yoshida, M. and Ozawa, E. (1990) Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem., 108, 748-752.
5. Ervasti, J.M. and Campbell, K.P. (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell, 66, 1121-1131.
6. Ervasti, J.M., Kahl, S.D. and Campbell, K.P. (1991) Purification of dystrophin from skeletal muscle. J. Biol. Chem., 266, 9161-9165.
7. Ohlendieck, K. and Campbell, K.P. (1991) Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J. Cell Biol., 115, 1685-1694.
8. Ervasti, J.M. andCampbell, K.P. (1993)Arole for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol., 122, 809-823.
9. 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.
10. Turner, P.R., Westwood, T., Regen, C.M. and Steinhardt, R.A. (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature, 335, 735-738.
11. Deconinck, N. and Dan, B. (2007) Pathophysiology of duchenne muscular dystrophy: current hypotheses. Pediatr. Neurol., 36, 1-7.
12. McArdle, A., Helliwell, T.R., Beckett, G.J., Catapano, M., Davis, A. and Jackson, M.J. (1998) Effect of propylthiouracil-induced hypothyroidism on the onset of skeletal muscle necrosis in dystrophin-deficient mdx mice. Clin. Sci. (Lond.), 95, 83-89.
13. Bulfield, G., Siller, W.G., Wight, P.A. and Moore, K.J. (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl Acad. Sci. USA, 81, 1189-1192.
14. Carnwath, J.W. and Shotton, D.M. (1987) Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J. Neurol. Sci., 80, 39-54.
15. Torres, L.F. and Duchen, L.W. (1987) The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain, 110, 269-299.
16. Coulton, G.R., Morgan, J.E., Partridge, T.A. and Sloper, J.C. (1988) The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol., 14, 53-70.
17. DiMario, J.X., Uzman, A. and Strohman, R.C. (1991) Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev. Biol., 148, 314-321.
18. Matsumura, K., Ervasti, J.M., Ohlendieck, K., Kahl, S.D. and Campbell, K.P. (1992) Association of dystrophin-related protein with dystrophinassociated proteins in mdx mouse muscle. Nature, 360, 588-591.
19. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Trickett, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
20. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J.M. and Davies, K. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med., 4, 1441-1444.
21. Burkin, D.J., Wallace, G.Q., Nicol, K.J., Kaufman, D.J. and Kaufman, S.J. (2001) Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J. Cell Biol., 152, 1207-1218.
22. Datta, S.R., Brunet, A. and Greenberg, M.E. (1999) Cellular survival: a play in three Akts. Genes Dev., 13, 2905-2927.
23. Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J.C., Glass, D.J. and Yancopoulos, G.D. (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol., 3, 1014-1019.
24. Rommel, C., Bodine, S.C., Clarke, B.A., Rossman, R., Nunez, L., Stitt, T.N., Yancopoulos, G.D. and Glass, D.J. (2001) Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol., 3, 1009-1013.
25. Pallafacchina,G., Calabria, E., Serrano, A.L., Kalhovde, J.M. and Schiaffino, S. (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc. Natl Acad. Sci. USA, 99, 9213-9218.
26. Takahashi, A., Kureishi, Y., Yang, J., Luo, Z., Guo, K., Mukhopadhyay, D., Ivashchenko, Y., Branellec, D. and Walsh, K. (2002) Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol. Cell Biol., 22, 4803-4814.
27. Rotwein, P. and Wilson, E.M. (2009) Distinct actions of Akt1 and Akt2 in skeletal muscle differentiation. J. Cell Physiol., 219, 503-511.
28. Peter, A.K. and Crosbie, R.H. (2006) Hypertrophic response of Duchenne and limb-girdle muscular dystrophies is associated with activation of Akt pathway. Exp. Cell Res., 312, 2580-2591.
29. Izumiya, Y., Hopkins, T., Morris, C., Sato, K., Zeng, L., Viereck, J., Hamilton, J.A., Ouchi, N., LeBrasseur, N.K. and Walsh, K. (2008) Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab., 7, 159-172.
30. Wagner, K.R., McPherron, A.C., Winik, N. and Lee, S.J. (2002) Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol., 52, 832-836.
31. Barton, E.R., Morris, L., Musaro, A., Rosenthal, N. and Sweeney, H.L. (2002) Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice. J. Cell Biol., 157, 137-148.
32. Burkin, D.J. and Kaufman, S.J. (1999) The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res., 296, 183-190.
33. Hodges, B.L., Hayashi, Y.K., Nonaka, I., Wang, W., Arahata, K. and Kaufman, S.J. (1997) Altered expression of the alpha7beta1 integrin in human and murine muscular dystrophies. J. Cell Sci., 110, 2873-2881.
34. Vachon, P.H., Xu, H., Liu, L., Loechel, F., Hayashi, Y., Arahata, K., Reed, J.C., Wewer, U.M. and Engvall, E. (1997) Integrins (alpha7beta1) in muscle function and survival. Disrupted expression in merosin-deficient congenital muscular dystrophy. J. Clin. Invest., 100, 1870-1881.
35. Cohn, R.D., Mayer, U., Saher, G., Herrmann, R., van der Flier, A., Sonnenberg, A., Sorokin, L. and Voit, T. (1999) Secondary reduction of alpha7B integrin in laminin alpha2 deficient congenital muscular dystrophy supports an additional transmembrane link in skeletal muscle. J. Neurol. Sci., 163, 140-152.
36. Khurana, T.S., Watkins, S.C., Chafey, P., Chelly, J., Tome, 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.
37. Peter, A.K., Ko, C.Y., Kim, M.H., Hsu, N., Ouchi, N., Rhie, S., Izumiya, Y., Zeng, L., Walsh, K. and Crosbie, R.H. (2009) Myogenic Akt signaling upregulates the utrophin-glycoprotein complex and promotes sarcolemma stability in muscular dystrophy. Hum. Mol. Genet., 18, 318-327.
38. Grill, M.A., Bales, M.A., Fought, A.N., Rosburg, K.C., Munger, S.J. and Antin, P.B. (2003) Tetracycline-inducible system for regulation of skeletal muscle-specific gene expression in transgenic mice. Transgenic Res., 12, 33-43.
39. Blake, D.J., Tinsley, J.M. and Davies, K.E. (1996) Utrophin: a structural and functional comparison to dystrophin. Brain Pathol., 6, 37-47.
40. Clerk, A., Morris, G.E., Dubowitz, V., Davies, K.E. and Sewry, C.A. (1993) Dystrophin-related protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem. J., 25, 554-561.
41. Lin, S. and Burgunder, J.M. (2000) Utrophin may be a precursor of dystrophin during skeletal muscle development. Brain Res. Dev. Brain Res., 119, 289-295.
42. Harris, J.B. (2003) Myotoxic phospholipases A2 and the regeneration of skeletal muscles. Toxicon, 42, 933-945.
43. Blaauw, B., Mammucari, C., Toniolo, L., Agatea, L., Abraham, R., Sandri, M., Reggiani, C. and Schiaffino, S. (2008) Akt activation prevents the force drop induced by eccentric contractions in dystrophin-deficient skeletal muscle. Hum. Mol. Genet., 17, 3686-3696.
44. Blaauw, B., Canato, M., Agatea, L., Toniolo, L., Mammucari, C., Masiero, E., Abraham, R., Sandri, M., Schiaffino, S. and Reggiani, C. (2009) Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J., 23, 3896-3905.
45. Webster, C., Silberstein, L., Hays, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
46. Gehrig, S.M., Koopman, R., Naim, T., Tjoakarfa, C. and Lynch, G.S. (2010) Making fast-twitch dystrophic muscles bigger protects them from contraction injury and attenuates the dystrophic pathology. Am. J. Pathol., 176, 29-33.
47. 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.
48. Cary, L.A. and Guan, J.L. (1999) Focal adhesion kinase in integrin-mediated signaling. Front. Biosci., 4, D102-D113.
49. Song, K.S., Scherer, P.E., Tang, Z., Okamoto, T., Li, S., Chafel, M., Chu, C., Kohtz, D.S. and Lisanti, M.P. (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J. Biol. Chem., 271, 15160-15165.
50. Yang, B., Jung, D., Motto, D., Meyer, J., Koretzky, G. and Campbell, K.P. (1995) SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem., 270, 11711-11714.
51. Hack, A.A., Cordier, L., Shoturma, D.I., Lam, M.Y., Sweeney, H.L. and McNally, E.M. (1999) Muscle degeneration without mechanical injury in sarcoglycan deficiency. Proc. Natl Acad. Sci. USA, 96, 10723-10728.
52. Hack, A.A., Ly, C.T., Jiang, F., Clendenin, C.J., Sigrist, K.S., Wollmann, R.L. and McNally, E.M. (1998) Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol., 142, 1279-1287.
53. Barton, E.R. (2006) Impact of sarcoglycan complex on mechanical signal transduction in murine skeletal muscle. Am. J. Physiol. Cell Physiol., 290, C411-C419.
54. Burkin, D.J., Wallace, G.Q., Milner, D.J., Chaney, E.J., Mulligan, J.A. and Kaufman, S.J. (2005) Transgenic expression of {alpha}7{beta}1 integrin maintains muscle integrity, increases regenerative capacity, promotes hypertrophy, and reduces cardiomyopathy in dystrophic mice. Am. J. Pathol., 166, 253-263.
55. Liu, J., Burkin, D.J. and Kaufman, S.J. (2008) Increasing alpha 7 beta 1-integrin promotes muscle cell proliferation, adhesion, and resistance to apoptosis without changing gene expression. Am. J. Physiol. Cell Physiol., 294, C627-C640.
56. Sander, M., Chavoshan, B., Harris, S.A., Iannaccone, S.T., Stull, J.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. USA, 97, 13818-13823.
57. Thomas, G.D., Shaul, P.W., Yuhanna, I.S., Froehner, S.C. and Adams, M.E. (2003) Vasomodulation by skeletal muscle-derived nitric oxide requires alpha-syntrophin-mediated sarcolemmal localization of neuronal nitric oxide synthase. Circ. Res., 92, 554-560.
58. Lai, Y., Thomas, G.D., Yue, Y., Yang, H.T., Li, D., Long, C., Judge, L., Bostick, B., Chamberlain, J.S., Terjung, R.L. and Duan, D. (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J. Clin. Invest., 119, 624-635.
59. 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.
60. 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., 123, 2008-2013.
61. Wilson, E.M., Hsieh, M.M. and Rotwein, P. (2003) Autocrine growth factor signaling by insulin-like growth factor-II mediates MyoD-stimulated myocyte maturation. J. Biol. Chem., 278, 41109-41113.
62. Wamhoff, B.R., Sinha, S. and Owens, G.K. (2007) Conditional mouse models to study developmental and pathophysiological gene function in muscle. Handb. Exp. Pharmacol., 178, 441-468.
63. Ouchi, N., Oshima, Y., Ohashi, K., Higuchi, A., Ikegami, C., Izumiya, Y. and Walsh, K. (2008) Follistatin-like 1, a secreted muscle protein, promotes endothelial cell function and revascularization in ischemic tissue through a nitric-oxide synthase-dependent mechanism. J. Biol. Chem., 283, 32802-32811.
64. Haugen, F., Norheim, F., Lian, H., Wensaas, A.J., Dueland, S., Berg, O., Funderud, A., Skalhegg, B.S., Raastad, T. and Drevon, C.A. (2010) IL-7 is expressed and secreted by human skeletal muscle cells. Am. J. Physiol. Cell Physiol., 298, C807-C816.
65. Melone, M.A., Peluso, G., Galderisi, U., Petillo, O. and Cotrufo, R. (2000) Increased expression of IGF-binding protein-5 in Duchenne muscular dystrophy (DMD) fibroblasts correlates with the fibroblast-induced downregulation of DMD myoblast growth: an in vitro analysis. J. Cell Physiol., 185, 143-153.
66. Liu, P., Cheng, H., Roberts, T.M. and Zhao, J.J. (2009) Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov., 8, 627-644.
67. Amalfitano, A. and Chamberlain, J.S. (1996) Themdx-amplification-resistant mutation system assay, a simple and rapid polymerase chain reaction-based detection of the mdx allele. Muscle Nerve, 19, 1549-1553.
68. Rooney, J.E., Welser, J.V., Dechert, M.A., Flintoff-Dye, N.L., Kaufman, S.J. and Burkin, D.J. (2006) Severe muscular dystrophy in mice that lack dystrophin and alpha7 integrin. J. Cell Sci., 119, 2185-2195.
69. Miller, G., Peter, A.K., Espinoza, E., Heighway, J. and Crosbie, R.H. (2006) Over-expression of Microspan, a novel component of the sarcoplasmic reticulum, causes severe muscle pathology with triad abnormalities. J. Muscle Res. Cell Motil., 27, 545-558.