Modulation of the dystrophin-associated protein complex in response to resistance training in young and older men

Journal of Applied Physiology

Volumn 104, Issue 5, 2008, Pages 1476-1484

  Kosek, David J ^a   Bamman, Marcas M ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

1 syntrophin; Caveolin 3; Mechanotransduction; Muscle hypertrophy; p38 mitogen activated protein kinase

Indexed keywords

CAVEOLIN 3; DYSTROPHIN; DYSTROPHIN ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NEURONAL NITRIC OXIDE SYNTHASE; CALCIUM BINDING PROTEIN; DYSTROBREVIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCLE PROTEIN; SYNTROPHIN ALPHA1;

ADULT; AGED; AGING; ARTICLE; CONTROLLED STUDY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; EXERCISE; HUMAN; HUMAN EXPERIMENT; MALE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE HYPERTROPHY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; BICYCLE; BIOSYNTHESIS; CELL SIZE; COLD; FITNESS; LUMINESCENCE; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; STRESS; ULTRASTRUCTURE; WESTERN BLOTTING;

ADULT; AGED; AGING; BICYCLING; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CAVEOLIN 3; CELL SIZE; COLD; DYSTROPHIN-ASSOCIATED PROTEINS; HUMANS; LUMINESCENCE; MALE; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE FIBERS; MUSCLE PROTEINS; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE I; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHYSICAL FITNESS; STRESS;

EID: 45149101295     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00708.2007     Document Type: Article

References (62)

1. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates PGC-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593, 2005.
2. Albrecht DE, Froehner SC. Syntrophins and dystrobrevins: defining the dystrophin scaffold at synapses. Neurosignals 11: 123-129, 2002.
3. Anderson JE. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 11: 1859-1874, 2000.
4. Anderson JE, Vargas C. Correlated NOS-IMU and Myf5 expression by satellite cells in mdx mouse muscle regeneration during NOS manipulation and deflazacort treatment. Neuromuscul Disord 13: 388-396, 2003.
5. Anderson JE, Wozniak AC. Satellite cell activation on fibers: modeling events in vivo-an invited review. Can J Physiol Pharmacol 82: 300-310, 2004.
6. Bamman MM, Ragan RC, Kim JS, Cross JM, Hill VJ, Tuggle SC, Allman RM. Myogenic protein expression before and after resistance loading in 26- and 64-yr-old men and women. J Appl Physiol 97: 1329-1337, 2004.
7. Bamman MM, Petrella JK, Kim JS, Mayhew DL, Cross JM. Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans. J Appl Physiol 102: 2232-2239, 2007.
8. Batchelor CL, Winder SJ. Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell Biol 16: 198-205, 2006.
9. Beaton LJ, Tarnopolsky MA, Phillips SM. Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol 544: 849-859, 2002.
10. Beggs AH, Byers TJ, Knoll JH, Boyce FM, Bruns GA, Kunkel LM. Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11. J Biol Chem 267: 9281-9288, 1992.
11. Biral D, Jakubiec-Puka A, Ciechomska I, Sandri M, Rossini K, Carraro U, Betto R. Loss of dystrophin and some dystrophin-associated proteins with concomitant signs of apoptosis in rat leg muscle overworked in extension. Acta Neuropathol (Berl) 100: 618-626, 2000.
12. 1-Integrin regulates mechanotransduction and prevents skeletal muscle injury. Am J Physiol Cell Physiol 290: C1660-C1665, 2006.
13. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743-752, 1995.
14. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS. Interaction of nitric oxide synthase with the postsynaptic density protein psd-95 and alpha1-syntrophin mediated by pdz domains. Cell 84: 757-767, 1996.
15. Burkin DJ, Wallace GQ, Milner DJ, Chaney EJ, Mulligan JA, Kaufman SJ. Transgenic expression of α7β1 integrin maintains muscle integrity, increases regenerative capacity, promotes hypertrophy, and reduces cardiomyopathy in dystrophic mice. Am J Pathol 166: 253-263, 2005.
16. Chao DS, Gorospe JR, Brenman JE, Rafael JA, Peters MF, Froehner SC, Hoffman EP, Chamberlain JS, Bredt DS. Selective loss of sarcolemmal nitric oxide synthase in Becker muscular dystrophy. J Exp Med 184: 609-618, 1996.
17. Chen ZP, McConell GK, Michell BJ, Snow RJ, Canny BJ, Kemp BE. AMPK signaling in contracting human skeletal muscle: acetyl-coa carboxylase and no synthase phosphorylation. Am J Physiol Endocrinol Metab 279: E1202-E1206, 2000.
18. Childs TE, Spangenburg EE, Vyas DR, Booth FW. Temporal alterations in protein signaling cascades during recovery from muscle atrophy. Am J Physiol Cell Physiol 285: C391-C398, 2003.
19. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 302: 1575-1577, 2003.
20. Croisier JL, Camus G, Venneman I, Deby-Dupont G, Juchmes-Ferir A, Lamy M, Crielaard JM, Deby C, Duchateau J. Effects of training on exercise-induced muscle damage and interleukin 6 production. Muscle Nerve 22: 208-212, 1999.
21. Evans W, Phinney S, Young V. Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14: 101-102, 1982.
22. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J Biol Chem 272: 25437-25440, 1997.
23. Grounds MD, Sorokin L, White J. Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 15: 381-391, 2005.
24. Hance JE, Fu SY, Watkins SC, Beggs AH, Michalak M. Alpha-actinin-2 is a new component of the dystrophin-glycoprotein complex. Arch Biochem Biophys 365: 216-222, 1999.
25. Hasegawa M, Cuenda A, Spillantini MG, Thomas GM, Buee-Scherrer V, Cohen P, Goedert M. Stress-activated protein kinase-3 interacts with the pdz domain of alpha1-syntrophin. A mechanism for specific substrate recognition. J Biol Chem 274: 12626-12631, 1999.
26. Hornberger TA, Esser KA. Mechanotransduction and the regulation of protein synthesis in skeletal muscle. Proc Nutr Soc 63: 331-335, 2004.
27. Iemitsu M, Maeda S, Jesmin S, Otsuki T, Kasuya Y, Miyauchi T. Activation pattern of MAPK signaling in the hearts of trained and untrained rats following a single bout of exercise. J Appl Physiol 101: 151-163, 2006.
28. Kadi F, Charifi N, Denis C, Lexell J, Andersen JL, Schjerling P, Olsen S, Kjaer M. The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflügers Arch 451: 319-327, 2005.
29. Kefaloyianni E, Gaitanaki C, Beis I. ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-kappaB transactivation during oxidative stress in skeletal myoblasts. Cell Signal 18: 2238-2251, 2006.
30. Kim JS, Cross JM, Bamman MM. Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women. Am J Physiol Endocrinol Metab 288: E1110-E1119, 2005.
31. Kim JS, Kosek DJ, Petrella JK, Cross JM, Bamman MM. Resting and load-induced levels of myogenic gene transcripts differ between older adults with demonstrable sarcopenia and young men and women. J Appl Physiol 99: 2149-2158, 2005.
32. Kosek DJ, Kim JS, Petrella JK, Cross JM, Bamman MM. Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol 101: 531-544, 2006.
33. Kubica N, Bolster DR, Farrell PA, Kimball SR, Jefferson LS. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2b epsilon mRNA in a mammalian target of rapamycin-dependent manner. J Biol Chem 280: 7570-7580, 2005.
34. Kumar A, Khandelwal N, Malya R, Reid MB, Boriek AM. Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J 18: 102-113, 2004.
35. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin 1/MAFbx in skeletal muscle. FASEB J 19: 362-370, 2005.
36. Lovering RM, De Deyne PG. Contractile function, sarcolemma integrity, and the loss of dystrophin after skeletal muscle eccentric contraction-induced injury. Am J Physiol Cell Physiol 286: C230-C238, 2004.
37. MacArthur DG, North KN. A gene for speed? The evolution and function of alpha-actinin-3. Bioessays 26: 786-795, 2004.
38. Madhavan R, Jarrett HW. Phosphorylation of dystrophin and alpha-syntrophin by Ca(2+)-calmodulin dependent protein kinase II. Biochim Biophys Acta 1434: 260-274, 1999.
39. Marsh DR, Criswell DS, Carson JA, Booth FW. Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats. J Appl Physiol 83: 1270-1275, 1997.
40. Marsh DR, Criswell DS, Hamilton MT, Booth FW. Association of insulin-like growth factor mRNA expressions with muscle regeneration in young, adult, and old rats. Am J Physiol Regul Integr Comp Physiol 273: R353-R358, 1997.
41. Martineau LC, Gardiner PF. Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91: 693-702, 2001.
42. Mount PF, Fraser SA, Watanabe Y, Lane N, Katsis F, Chen ZP, Kemp BE, Power DA. Phosphorylation of neuronal and endothelial nitric oxide synthase in the kidney with high and low salt diets. Nephron Physiol 102: p36-p50, 2005.
43. Petrella JK, Kim JS, Tuggle SC, Hall SR, Bamman MM. Age differences in knee extension power, contractile velocity, and fatigability. J Appl Physiol 98: 211-220, 2005.
44. Petrella JK, Kim JS, Cross JM, Kosek DJ, Bamman MM. Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab 291: E937-E946, 2006.
45. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710-3714, 1993.
46. Ploutz-Snyder LL, Giamis EL, Formikell M, Rosenbaum AE. Resistance training reduces susceptibility to eccentric exercise-induced muscle dysfunction in older women. J Gerontol A Biol Sci Med Sci 56: B384-B390, 2001.
47. Psilander N, Damsgaard R, Pilegaard H. Resistance exercise alters MRF and IGF-I mRNA content in human skeletal muscle. J Appl Physiol 95: 1038-1044, 2003.
48. Smith LW, Smith JD, Criswell DS. Involvement of nitric oxide synthase in skeletal muscle adaptation to chronic overload. J Appl Physiol 92: 2005-2011, 2002.
49. Suelves M, Lluis F, Ruiz V, Nebreda AR, Munoz-Canoves P. Phosphorylation of MRF4 transactivation domain by p38 mediates repression of specific myogenic genes. EMBO J 23: 365-375, 2004.
50. Sunada Y, Ohi H, Hase A, Hosono T, Arata S, Higuchi S, Matsumura K, Shimizu T. Transgenic mice expressing mutant caveolin-3 show severe myopathy associated with increased nNOS activity. Hum Mol Genet 10: 173-178, 2001.
51. Tatsumi R, Hattori A, Ikeuchi Y, Anderson JE, Allen RE. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of ph and nitric oxide. Mol Biol Cell 13: 2909-2918, 2002.
52. Tatsumi R, Liu X, Pulido A, Morales M, Sakata T, Dial S, Hattori A, Ikeuchi Y, Allen RE. Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am J Physiol Cell Physiol 290: C1487-C1494, 2006.
53. Tidball JG, Lavergne E, Lau KS, Spencer MJ, Stull JT, Wehling M. Mechanical loading regulates NOS expression and activity in developing and adult skeletal muscle. Am J Physiol Cell Physiol 275: C260-C266, 1998.
54. Towler MC, Kaufman SJ, Brodsky FM. Membrane traffic in skeletal muscle. Traffic 5: 129-139, 2004.
55. Venema VJ, Ju H, Zou R, Venema RC. Interaction of neuronal nitricoxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem 272: 28187-28190, 1997.
56. Wakayama Y, Inoue M, Murahashi M, Shibuya S, Jimi T, Kojima H, Oniki H. Ultrastructural localization of alpha 1-syntrophin and neuronal nitric oxide synthase in normal skeletal myofiber, and their relation to each other and to dystrophin. Acta Neuropathol (Berl) 94: 455-464, 1997.
57. Welle S, Thornton C, Statt M. Myofibrillar protein synthesis in young and old human subjects after three months of resistance training. Am J Physiol Endocrinol Metab 268: E422-E427, 1995.
58. Williamson D, Gallagher P, Harber M, Hollon C, Trappe S. Mitogen-activated protein kinase (MAPK) pathway activation: effects of age and acute exercise on human skeletal muscle. J Physiol 547: 977-987, 2003.
59. Willoughby DS, Nelson MJ. Myosin heavy-chain mRNA expression after a single session of heavy-resistance exercise. Med Sci Sports Exerc 34: 1262-1269, 2002.
60. Woolstenhulme MT, Conlee RK, Drummond MJ, Stites AW, Parcell AC. Temporal response of desmin and dystrophin proteins to progressive resistance exercise in human skeletal muscle. J Appl Physiol 100: 1876-1882, 2006.
61. Yarasheski KE, Pak-Loduca J, Hasten DL, Obert KA, Brown MB, Sinacore DR. Resistance exercise training increases mixed muscle protein synthesis rate in frail women and men ≥76 yr old. Am J Physiol Endocrinol Metab 277: E118-E125, 1999.
62. Yu M, Blomstrand E, Chibalin AV, Krook A, Zierath JR. Marathon running increases ERK1/2 and p38 MAP kinase signalling to downstream targets in human skeletal muscle. J Physiol 536: 273-282, 2001.