Interaction between signalling pathways involved in skeletal muscle responses to endurance exercise

Pflugers Archiv European Journal of Physiology

Volumn 452, Issue 2, 2006, Pages 125-139

  Koulmann, Nathalie ^a   Bigard, André Xavier ^a  

^a CENTRE DE RECHERCHES   (France)

Author keywords

Fibre type switching; HIF 1; Hypoxia; MAPK; MEF2; Mitochondrial biogenesis; Myosin heavy chain; NFAT

Indexed keywords

CALCIUM; CALPAIN; MITOGEN ACTIVATED PROTEIN KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE (CALCIUM,CALMODULIN);

BIOGENESIS; CYTOSOL; ENDURANCE; ENERGY METABOLISM; ENZYME ACTIVATION; EXERCISE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; MEDICAL LITERATURE; MOLECULAR DYNAMICS; MUSCLE FIBRIL; NEUROMUSCULAR FUNCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANOXIA; EXERCISE; GENE EXPRESSION; HUMANS; MUSCLE FIBERS; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHENOTYPE; PHYSICAL ENDURANCE; SIGNAL TRANSDUCTION;

EID: 33745822807     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-005-0030-9     Document Type: Review

References (140)

1. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z (2005) Exercise stimulates PGC-1α transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280:19587-19593
2. 2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol 287:C1311-C1319
3. Allen DL, Leinwand LA (2002) Intracellular calcium and myosin isoform transitions. Calcineurin and calcium-calmodulin kinase pathways regulate preferential activation of the IIa myosin heavy chain promoter. J Biol Chem 277:45323-45330
4. Ameln H, Gustaffsson T, Sundberg CJ, Okamoto K, Jansson E, Poellinger L, Makino Y (2005) Physiological activation of hypoxia inducible factor-1 in human skeletal muscle. FASEB J 19:1009-1011
5. Andersen P, Henriksson J (1977) Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol 270:677-690
6. Andersen JL, Schjerling P, Saltin B (2000) Muscle, genes, and athletic performance. Sci Am 283:48-55
7. Atherton PJ, Babraj JA, Smith K, Singh J, Rennie MJ, Wackerhage H (2005) Selective activation of AMPK-PGC-1α or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19:786-788
8. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO (2002) Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16:1879-1886
9. Banzet S, Koulmann N, Simler N, Birot O, Sanchez H, Chapot R, Peinnequin A, Bigard X (2005) Fibre type specificity of IL-6 gene transcription during muscle contraction in rat: association with calcineurin activity. J Physiol 566:839-847
10. Bassel-Duby R, Olson EN (2003) Role of calcineurin in striated muscle: development, adaptation, and disease. Biochem Biophys Res Commun 311:1133-1141
11. Bigard AX, Sanchez H, Zoll J, Mateo P, Rousseau V, Veksler V, Ventura-Clapier R (2000) Calcineurin co-regulates contractile and metabolic components of slow muscle phenotype. J Biol Chem 275:19653-19660
12. Bigard AX, Mateo P, Sanchez H, Serrurier B, Ventura-Clapier R (2000) Lack of coordinated changes in metabolic enzymes and myosin heavy chain isoforms in regenerated muscles of trained rats. J Muscle Res Cell Motil 21:269-278
13. Birot OJG, Koulmann N, Peinnequin A, Bigard XA (2003) Exercise-induced expression of vascular endothelial growth factor mRNA in rat skeletal muscle is dependent on fibre type. J Physiol 552:213-221
14. Bonen A (2000) Lactate transporters (MCT proteins) in heart and skeletal muscles. Med Sci Sports Exerc 32:778-789
15. 2-terminal kinase activity in human skeletal muscle. J Appl Physiol 87:1668-1673
16. 2-terminal kinase activity and p38 phosphorylation in rat skeletal muscle. Am J Physiol 280:C352-C358
17. Botinelli R, Reggiani C (2000) Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73:195-262
18. Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417-439
19. Bunn HF, Poyton RO (1996) Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76:839-885
20. Calvo S, Venepally P, Cheng J, Buonanno A (1999) Fiber-type-specific transcription of the troponin I slow gene is regulated by multiple elements. Mol Cell Biol 19:515-525
21. Carrasco MA, Riveros N, Rios J, Muller M, Torres F, Pineda J, Landatilla S, Jaimovich E (2003) Depolarization-induced slow calcium transients activate early genes in skeletal muscle cells. Am J Physiol Cell Physiol 284:C1438-C1447
22. Chakkalakal JV, Stocksley MA, Harrison MA, Angus LM, Deschenes-Furry J, St-Pierre S, Megeney LA, Chin ER, Michel RN, Jasmin BJ (2003) Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signalling. Proc Natl Acad Sci USA 100:7791-7796
23. Chin ER, Olson EN, Yang Q, Shelton JM, Bassel-Duby R, Williams RS (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12:2499-2509
24. 2+/calmodulin-dependent kinases in skeletal muscle plasticity. J Appl Physiol 99:414-423
25. Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270-283
26. Demirel HA, Powers SK, Naito H, Hugues M, Coombes JS (1999) Exercise-induced alterations in skeletal muscle myosin heavy chain phenotype: dose response relationship. J Appl Physiol 86:1002-1008
27. Dentel JN, Blanchard SG, Ankrapp DP, McCabe LR, Wiseman RW (2005) Inhibition of cross-bridge formation has no effect on contraction-associated phosphorylation of p38 MAPK in mouse skeletal muscle. Am J Physiol 288:C824-C830
28. 2+ response amplitude and duration. Nature 386:855-858
29. Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC, Brooks G (2000) Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab 278:E571-E579
30. Dunn SE, Bums JL, Michel RN (1999) Calcineurin is required for skeletal muscle hypertrophy. J Biol Chem 274:21908-21912
31. Ekmark M, Gronevik E, Schjerling P, Gundersen K (2003) Myogenin induces higher oxidative capacity in pre-existing mouse muscle fibres after somatic DNA transfer. J Physiol 548:259-269
32. Faller D (1999) Endothelial cell responses to hypoxic stress. Clin Exp Pharmacol Physiol 26:74-84
33. Flück M, Hoppeler H (2003) Molecular basis of skeletal muscle plasticity - from gene to form and function. Rev Physiol Biochem Pharmacol 146:159-216
34. 2+-independent kinase activity increases during either hypertrophy or running. J Appl Physiol 88:352-358
35. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by the hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613
36. Freyssenet D, Di Carlo M, Hood DA (1999) Calcium-dependent regulation of cytochrome c gene expression in skeletal muscle cells. J Biol Chem 274:9305-9311
37. Friday BB, Horsley V, Pavlath GK (2000) Calcineurin activity is required for the initiation of skeletal muscle differentiation. J Cell Biol 149:657-666
38. Frosig C, Jorgensen SB, Hardie DG, Richter EA, Wojtaszewski JFP (2004) 5′-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle. Am J Physiol 286:E411-E417
39. Galler S, Schmitt TL, Hilber K, Pette D (1997) Stretch activation and isoforms of myosin heavy chain and troponin-T of rat skeletal muscle fibres. J Muscle Res Cell Motil 18:555-561
40. Gamier A, Fortin D, Zoll J, N'Guessan B, Mettauer B, Lampert E, Veksler V, Ventura-Clapier R (2005) Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle. FASEB J 19:43-52
41. Gavin TP, Spector DA, Wagner H, Breen EC, Wagner PD (2000) Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise. J Appl Physiol 88:1192-1198
42. Gayeski TEJ, Connett RJ, Honig CR (1985) Oxygen transport in rest-work transition illustrates new functions for myoglobin. Am J Physiol 248:H914-H921
43. Gerber H-P, Condorelli F, Park J, Ferrara N (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. J Biol Chem 272:23659-23667
44. Giger JM, Haddad F, Qin AX, Baldwin KM (2004) Effect of cyclosporin A treatment on the in vivo regulation of type I MHC gene expression. J Appl Physiol 97:475-483
45. Gilde AJ, van Bilsen M (2003) Peroxisome proliferator-activated receptors (PPARs): regulators of gene expression in heart and skeletal muscle. Acta Physiol Scand 178:425-434
46. Glass DJ (2003) Molecular mechanisms modulating muscle mass. Trends Mol Med 9:344-350
47. Goldspink G (2002) Gene expression in skeletal muscle. Biochem Soc Trans 30:285-290
48. Goodyear L, Chang PY, Sherwood D, Dufresne S, Moller D (1996) Effects of exercise and insulin on mitogen-activated protein kinase signaling pathways in rat skeletal muscle. Am J Physiol 271:E403-E408
49. Gundersen K (1998) Determination of muscle contractile properties: the importance of the nerve. Acta Physiol Scand 162:333-341
50. Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ (1999) Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol 276:H679-685
51. Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor γ coactivator 1α expression in muscle. Proc Natl Acad Sci USA 100:7111-7116
52. Helgren ME (1994) Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76:493-504
53. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320-327
54. Howald H, Hoppeler H, Claasen H, Mathieu O, Straub R (1985) Influences of endurance training on the structural composition of the different muscle fiber types in humans. Pflügers Arch 403:369-376
55. Huang CF, Tong J, Schmidt J (1992) Protein kinase C couples membrane excitation to acetylcholine receptor gene inactivation in chick skeletal muscle. Neuron 9:671-678
56. Jostarndt-Fögen K, Puntschart A, Hoppeler H, Billeter R (1998) Fibre-type specific expression of fast and slow essential myosin light chain mRNAs in trained human skeletal muscles. Acta Physiol Scand 164:299-308
57. Kallio PJ, Okamoto K, O'Brien S, Carrero P, Makino Y, Tanaka H, Poellinger L (1998) Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J 17:6573-6586
58. Karin M, Liu Z, Zandi E (1997) AP-1 function and regulation. Curr Opin Cell Biol 9:240-246
59. Kostrominova TY, MacPherson PCD, Carlson BM, Goldman D (2000) Regulation of myogenin protein expression in denervated muscles from young and old rats. Am J Physiol 279:R179-R188
60. 2+ transients activate calcineurin/NFATc1 and initiate fast-to-slow transformation in a primary skeletal muscle culture. Am J Physiol 285:C56-C63
61. Kubo H, Libonati JR, Kendrick ZV, Paolone A, Gaughan JP, Houser SR (2003) Differential effects of exercise training on skeletal muscle SERCA gene expression. Med Sci Sports Exerc 35:27-31
62. Kumar A, Chaudhry I, Reid MB, Boriek AM (2002) Distinct signaling pathways are activated in response to mechanical stress applied axially and transversally to skeletal muscle fibers. J Biol Chem 277:46493-46503
63. Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscle. J Physiol 472:595-614
64. 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 (2002) Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418:797-801
65. Liu Y, Cseresnyes Z, Randall WR, Schneider MF (2001) Activity-dependent nuclear translocation and intranuclear distribution of NFATc in adult skeletal muscle fibers. J Cell Biol 155:27-39
66. Long YC, Widegren U, Zierath JR (2004) Exercise-induced mitogen-activated protein kinase signalling in skeletal muscle. Proc Nutr Soc 63:227-232
67. Market CL (1962) Lactate dehydrogenase isozymes: dissociation and recombination of subunits. Science 140:1329-1330
68. Martineau LC, Gardiner PF (2001) Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91:693-702
69. Mason SD, Howlett RA, Kim MJ, Olfert M, Hogan MC, McNulty W, Hickey RP, Wagner PD, Kahn RC, Giordano FJ, Johnson RS (2004) Loss of skeletal muscle HIF-1α results in altered exercise endurance. PLoS Biol 2:e288
70. McCullagh KJA, Poole RC, Halestrap AP, O'Brien M, Bonen A (1996) Role of lactate transporter (MCT1) in skeletal muscles. Am J Physiol 271:E143-E150
71. McGee SL, Hargreaves M (2004) Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes 53:1208-1214
72. McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27:40-47
73. McKinsey TA, Zhang CL, Olson EN (2000) Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci USA 97:14400-14405
74. Megeney LA, Prasad M, Tan MH, Bonen A (1994) Expression of the insulin-regulable transporter GLUT-4 is influenced by neurogenic factors. Am J Physiol 266:E813-E816
75. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, Lehman JJ, Kelly DP, Spiegelman BM (2001) Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci USA 98:3820-3825
76. Minet E, Michel G, Mottet D, Raes M, Michiels C (2001) Transduction pathways involved in hypoxia-inducible factor-1 phosphorylation and activation. Free Radic Biol Med 31:847-855
77. Murgia M, Serrano AL, Calabria E, Pallafacchina G, Lømo T, Schiaffino S (2000) Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat Cell Biol 2:142-147
78. Nader GA, Esser KA (2001) Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90:1936-1942
79. Naya FJ, Mercer B, Shelton J, Richardson JA, Williams RS, Olson EN (2000) Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J Biol Chem 275:4545-4548
80. Nielsen JN, Frosig C, Sajan MP, Miura A, Standaert ML, Graham DA, Wojtaszewski JFP, Farese RV, Richter EA (2003) Increased atypical PKC activity in endurance-trained human skeletal muscle. Biochem Biophys Res Commun 312:1147-1153
81. Norrbom J, Sundberg CJ, Ameln H, Kraus WE, Jansson E, Gustafsson T (2004) PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J Appl Physiol 96:189-194
82. O'Neil DS, Zheng D, Anderson WK, Dohm GL, Houmard JA (1999) Effect of endurance exercise on myosin heavy chain gene regulation in human skeletal muscle. Am J Physiol 276:R414-R419
83. Ozawa K, Kondo T, Hori O, Kitao Y, Stem DM, Eisenmenger W, Ogawa S, Ohshima T (2001) Expression of the oxygen-regulated protein ORP-150 accelerates wound healing by modulating intracellular VEGF transport. J Clin Invest 108:41-50
84. Parry DJ (2001) Myosin heavy chain expression and plasticity: role of myoblast diversity. Exerc Sport Sci Rev 29:175-179
85. Parsons SA, Wilkins BJ, Bueno OF, Molkentin JD (2003) Altered skeletal muscle phenotypes in calcineurin Aalpha and Abeta gene-targeted mice. Mol Cell Biol 23:4331-4343
86. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153-183
87. Pette D (1998) Training effects on the contractile apparatus. Acta Physiol Scand 162:367-376
88. Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types and transitions. Microsc Res Tech 50:500-509
89. Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115-202
90. Pette D, Vrbova G (1999) What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve 22:666-667
91. Phillips SM, Han XX, Green HJ, Bonen A (1996) Increments in skeletal muscle GLUT-1 and GLUT-4 after endurance training in humans. Am J Physiol 270:E456-E462
92. Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC1α gene in human skeletal muscle. J Physiol 546:851-858
93. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839
94. Rao A, Luo C, Hogan PG (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707-747
95. Rivero JL, Talmadge RJ, Edgerton VR (1999) Interrelationships of myofibrillar ATPase activity and metabolic properties of myosin heavy chain-based fibre types in rat skeletal muscle. Histochem Cell Biol 111:277-287
96. Roberts KC, Nixon C, Unthank JL, Lash JL (1997) Femoral artery ligation stimulates capillary growth and limits training-induced increases in oxidative capacity in rats. Microcirculation 4:253-260
97. Rothermel B, Vega RB, Yang J, Wu H, Bassel-Duby R, Williams RS (2000) A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J Biol Chem 275:8719-8725
98. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, Gobelet C, Meier CA, Bell DR, Kralli A, Giacobino JP, Deriaz O (2003) Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor γ coactivator-1 and peroxisome proliferator-activated receptor-α in skeletal muscle. Diabetes 52:2874-2881
99. Ryder JW, Bassel-Duby R, Olson EN, Zierath JR (2003) Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278:44298-44304
100. Ryder JW, Fahlman R, Wallberg-Henriksson H, Alessi DR, Krook A, Zierath JR (2000) Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. J Biol Chem 275:1457-1462
101. Salviati G, Betto R, Danieli-Betto D, Zeviani M (1984) Myofibrillar protein isoforms and sarcoplasmic reticulum calcium-transport activity of single human muscle fibres. Biochem J 224:215-225
102. Sanchez H, N'Guessan B, Ribera F, Ventura-Clapier R, Bigard AX (2003) The cyclosporin A treatment increases the oxidative capacity of soleus muscle in rats. Muscle Nerve 28:324-329
103. Scarpulla RC (2002) Transcriptional activators and co-activators in the nuclear control of mitochondrial function in mammalian cells. Gene 286:81-89
104. Schantz PG, Dhoot GK (1987) Co-existence of slow and fast isoforms of contractile and regulatory proteins in human skeletal muscle fibres induced by endurance training. Acta Physiol Scand 131:147-154
105. Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Phys Rev 76:371-423
106. Schmitt B, Flück M, Décombaz J, Kreis R, Boesch C, Wittwer M, Graber F, Vogt M, Howald H, Hoppeler H (2003) Transcriptional adaptations of lipid metabolism in tibialis anterior muscle of endurance-trained athletes. Physiol Genomics 15:148-157
107. Semenza GL (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19:176-182
108. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, Giallongo A (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor-1. J Biol Chem 271:32529-32537
109. Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lømo T, Schiaffino S (2001) Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci USA 98:13108-13113
110. Siu PM, Donley DA, Bryner RW, Always SE (2004) Myogenin and oxidative enzyme gene expression levels are elevated in rat soleus muscles after endurance training. J Appl Physiol 97:277-285
111. Smerdu V, Karsch-Mizrachi I, Campione M, Leinwand L, Schiaffino S (1994) Type IIx myosin heavy chain transcripts are expressed in type IIb fibers of human skeletal muscle. Am J Physiol 267:C1723-C1728
112. Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413-424
113. Swoap SJ, Hunter SB, Stevenson EJ, Felton HM, Kansagra NV, Lang JM, Esser KA, Kandarian SC (2000) The calcineurin-NFAT pathway and muscle fiber-type gene expression. Am J Physiol 279:C915-C924
114. Talmadge RJ, Otis JS, Rittler MR, Garcia ND, Spencer SR, Lees SJ, Naya FJ (2004) Calcineurin activation influences muscle phenotype in a muscle-specific fashion. BMC Cell Biology 5:28
115. Terrada S, Goto M, Kato M, Kawanaka K, Shimokawa T, Tabata I (2002) Effects of low-intensity prolonged exercise on PGC1-1 mRNA expression in rat epitrochlearis muscle. Biochem Biophys Res Commun 296:350-354
116. 2+-ATPase. Biochem J 329:131-136
117. Thompson HS, Maynard EB, Morales ER, Scordilis SP (2003) Exercise-induced HSP27, HSP70 and MAPK responses in human skeletal muscle. Acta Physiol Scand 178:61-72
118. Ventura-Clapier R, Veksler V, Hoerter JA (1994) Myofibrillar creatine kinase and cardiac contraction. Mol Cell Biochem 133-134:125-144
119. Wada M, Pette D (1993) Relationship between alkali light chain complement and myosin heavy chain isoforms in single fast twitch fibres of rat and rabbit. Eur J Biochem 214:157-161
120. 2 transport in muscle. Acta Physiol Scand 168:609-614
121. Walters EH, Stickland NC, Loughna PT (2000) The expression of the myogenic regulatory factors in denervated and normal muscles of different phenotypes. J Muscle Res Cell Motil 21:647-653
122. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM (2004) Regulation of muscle fiber type and running endurance by PPARδ. PLoS Biol 2(10):e294
123. Weis J, Kaussen M, Calvo S, Buonanno A (2000) Denervation induces a rapid nuclear accumulation of MRF4 in mature myofibers. Dev Dyn 218:438-451
124. 2-regulated gene. FASEB J 16:1151-1162
125. Widegren U, Liang X, Krook A, Chivalin AV, Bjornholm M, Tally M, Roth RA, Henriksson J, Zierath JR (1998) Divergent effects of exercise on metabolic and mitogenic signaling pathways in human skeletal muscle. FASEB J 12:1379-1389
126. Windisch A, Gundersen K, Szabolcs MJ, Gruber H, Lomo T (1998) Fast to slow transformation of denervated and electrically stimulated rat muscle. J Physiol 510:623-632
127. Winder WW, Holmes BF, Rubink DS, Jensen EB, Chen M, Holloszy JO (2000) Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88:2219-2226
128. Witmarsh AJ, Davis RJ (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74:589-607
129. Wretman C, Lionikas A, Widegren U, Lannergren J, Westerblad H, Hanriksson J (2001) Effects of concentric and eccentric contractions on phosphorylation of MAPK (erk1/2) and MAPK(p38) in isolated rat skeletal muscle. J Physiol 535: 155-164
130. Wu Z, Puisgsever P, Anderson U, Zhang C, Adelmant G, Moother V, Troy A, Cinti S, Lowell B, Scarpulla RC, Speigelman BM (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124
131. Wu H, Naya FJ, Mc Kinsey TA, Mercer B, Shelton JM, Chin ER, Simard AR, Michel RN, Bassel-Duby R, Olson EN, Williams RS (2000) MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J 19:1963-1973
132. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson JA, DiMaio JM, Olson EN, Bassel-Duby R, Willimas RS (2001) Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20:414-6423
133. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349-352
134. Yang SH, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320:3-21
135. York JW, Oscai LB, Penney DG (1974) Alterations in skeletal muscle lactate dehydrogenase isozymes following exercise training. Biochem Biophys Res Commun 61:1387-1393
136. Yu M, Blomstrand E, Chibalin AV, Krook A, Zierath JR (2001) Marathon running increases ERK1/2 and p38 MAP kinase signalling to downstream targets in human skeletal muscle. J Physiol 536:273-282
137. Yu M, Stepto NK, Chibalin AV, Fryer LGD, Carling D, Krook A, Hawley JA, Zierath JR (2003) Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J Physiol 546:327-335
138. Zhao M, New L, Kravchenko VV, Kato Y, Gram H, di Padova F, Olson EN, Ulevitch RJ, Han J (1999) Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol 19:21-30
139. Zoll J, Koulmann N, Bahi L, Ventura-Clapier R, Bigard AX (2003) Quantitative and qualitative adaptation of skeletal muscle mitochondria to increased physical activity. J Cell Physiol 194:186-193
140. Zoll J, Sanchez H, N'Guessan B, Ribera F, Lampert E, Bigard AX, Serrurier B, Fortin D, Geny B, Veksler V, Ventura-Clapier R, Mettauer B (2002) Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J Physiol 543:191-200