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Pflügers Archiv

, 452:125 | Cite as

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

  • Nathalie Koulmann
  • André-Xavier BigardEmail author
Invited Review

Abstract

The purpose of this review is to summarise the latest literature on the signalling pathways involved in transcriptional modulations of genes that encode contractile and metabolic proteins in response to endurance exercise. A special attention has been paid to the cooperation between signalling pathways and coordinated expression of protein families that establish myofibre phenotype. Calcium acts as a second messenger in skeletal muscle during exercise, conveying neuromuscular activity into changes in the transcription of specific genes. Three main calcium-triggered regulatory pathways acting through calcineurin, Ca2+–calmodulin-dependent protein kinases (CaMK) and Ca2+-dependent protein kinase C, transduce alterations in cytosolic calcium concentration to target genes. Calcineurin signalling, the most important of these Ca2+-dependent pathways, stimulates the activation of many slow-fibre gene expression, including genes encoding proteins involved in contractile process, Ca2+ uptake and energy metabolism. It involves the interaction between multiple transcription factors and the collaboration of other Ca2+-dependent CaMKs. Although members of mitogen-activated protein kinase (MAPK) pathways are activated during exercise, their integration into other signalling pathways remains largely unknown. The peroxisome proliferator-activated receptor γ (PPARγ) coactivator-1α (PGC-1α) constitutes a pivotal factor of the circuitry which coordinates mitochondrial biogenesis and which couples to the expression of contractile and metabolic genes with prolonged exercise.

Keywords

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

References

  1. 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 280:19587–19593PubMedGoogle Scholar
  2. 2.
    Akimoto T, Ribar TJ, Williams RS, Yan Z (2004) Skeletal muscle adaptation in response to voluntary running in Ca2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol 287:C1311–C1319Google Scholar
  3. 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 277:45323–45330PubMedGoogle Scholar
  4. 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 19:1009–1011PubMedGoogle Scholar
  5. 5.
    Andersen P, Henriksson J (1977) Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol 270:677–690PubMedGoogle Scholar
  6. 6.
    Andersen JL, Schjerling P, Saltin B (2000) Muscle, genes, and athletic performance. Sci Am 283:48–55PubMedCrossRefGoogle Scholar
  7. 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 19:786–788PubMedGoogle Scholar
  8. 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 16:1879–1886PubMedGoogle Scholar
  9. 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 566:839–847PubMedGoogle Scholar
  10. 10.
    Bassel-Duby R, Olson EN (2003) Role of calcineurin in striated muscle: development, adaptation, and disease. Biochem Biophys Res Commun 311:1133–1141PubMedGoogle Scholar
  11. 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 275:19653–19660PubMedGoogle Scholar
  12. 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 21:269–278PubMedGoogle Scholar
  13. 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 552:213–221PubMedGoogle Scholar
  14. 14.
    Bonen A (2000) Lactate transporters (MCT proteins) in heart and skeletal muscles. Med Sci Sports Exerc 32:778–789PubMedGoogle Scholar
  15. 15.
    Boppart MD, Aronson D, Gibson L, Roubenoff R, Abad LW, Bean J, Goodyear LJ, Fielding RA (1999) Eccentric exercise markedly increases c-Jun NH2-terminal kinase activity in human skeletal muscle. J Appl Physiol 87:1668–1673PubMedGoogle Scholar
  16. 16.
    Boppart MD, Hirshman MF, Sakamoto K, Fielding RA, Goodyear LJ (2001) Static stretch increases c-Jun NH2-terminal kinase activity and p38 phosphorylation in rat skeletal muscle. Am J Physiol 280:C352–C358Google Scholar
  17. 17.
    Botinelli R, Reggiani C (2000) Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 73:195–262Google Scholar
  18. 18.
    Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417–439PubMedGoogle Scholar
  19. 19.
    Bunn HF, Poyton RO (1996) Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76:839–885PubMedGoogle Scholar
  20. 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 19:515–525PubMedGoogle Scholar
  21. 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–C1447PubMedGoogle Scholar
  22. 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 100:7791–7796PubMedGoogle Scholar
  23. 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 12:2499–2509PubMedGoogle Scholar
  24. 24.
    Chin ER (2005) Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity. J Appl Physiol 99:414–423PubMedGoogle Scholar
  25. 25.
    Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283PubMedGoogle Scholar
  26. 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 86:1002–1008PubMedGoogle Scholar
  27. 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–C830Google Scholar
  28. 28.
    Dolmetsh RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386:855–858Google Scholar
  29. 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–E579PubMedGoogle Scholar
  30. 30.
    Dunn SE, Burns JL, Michel RN (1999) Calcineurin is required for skeletal muscle hypertrophy. J Biol Chem 274:21908–21912PubMedGoogle Scholar
  31. 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 548:259–269PubMedGoogle Scholar
  32. 32.
    Faller D (1999) Endothelial cell responses to hypoxic stress. Clin Exp Pharmacol Physiol 26:74–84PubMedGoogle Scholar
  33. 33.
    Flück M, Hoppeler H (2003) Molecular basis of skeletal muscle plasticity—from gene to form and function. Rev Physiol Biochem Pharmacol 146:159–216PubMedGoogle Scholar
  34. 34.
    Flück M, Waxham MN, Hamilton MT, Booth FW (2000) Skeletal muscle Ca2+-independent kinase activity increases during either hypertrophy or running. J Appl Physiol 88:352–358PubMedGoogle Scholar
  35. 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 16:4604–4613PubMedGoogle Scholar
  36. 36.
    Freyssenet D, Di Carlo M, Hood DA (1999) Calcium-dependent regulation of cytochrome c gene expression in skeletal muscle cells. J Biol Chem 274:9305–9311PubMedGoogle Scholar
  37. 37.
    Friday BB, Horsley V, Pavlath GK (2000) Calcineurin activity is required for the initiation of skeletal muscle differentiation. J Cell Biol 149:657–666PubMedGoogle Scholar
  38. 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–E417Google Scholar
  39. 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 18:555–561PubMedGoogle Scholar
  40. 40.
    Garnier 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 19:43–52PubMedGoogle Scholar
  41. 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 88:1192–1198PubMedGoogle Scholar
  42. 42.
    Gayeski TEJ, Connett RJ, Honig CR (1985) Oxygen transport in rest–work transition illustrates new functions for myoglobin. Am J Physiol 248:H914–H921PubMedGoogle Scholar
  43. 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 272:23659–23667PubMedGoogle Scholar
  44. 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 97:475–483PubMedGoogle Scholar
  45. 45.
    Gilde AJ, van Bilsen M (2003) Peroxisome proliferator-activated receptors (PPARs): regulators of gene expression in heart and skeletal muscle. Acta Physiol Scand 178:425–434PubMedGoogle Scholar
  46. 46.
    Glass DJ (2003) Molecular mechanisms modulating muscle mass. Trends Mol Med 9:344–350PubMedGoogle Scholar
  47. 47.
    Goldspink G (2002) Gene expression in skeletal muscle. Biochem Soc Trans 30:285–290PubMedGoogle Scholar
  48. 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–E408PubMedGoogle Scholar
  49. 49.
    Gundersen K (1998) Determination of muscle contractile properties: the importance of the nerve. Acta Physiol Scand 162:333–341PubMedGoogle Scholar
  50. 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:H679–685PubMedGoogle Scholar
  51. 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 100:7111–7116PubMedGoogle Scholar
  52. 52.
    Helgren ME (1994) Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76:493–504PubMedGoogle Scholar
  53. 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 59:320–327PubMedGoogle Scholar
  54. 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 403:369–376PubMedGoogle Scholar
  55. 55.
    Huang CF, Tong J, Schmidt J (1992) Protein kinase C couples membrane excitation to acetylcholine receptor gene inactivation in chick skeletal muscle. Neuron 9:671–678PubMedGoogle Scholar
  56. 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 164:299–308PubMedGoogle Scholar
  57. 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 17:6573–6586PubMedGoogle Scholar
  58. 58.
    Karin M, Liu Z, Zandi E (1997) AP-1 function and regulation. Curr Opin Cell Biol 9:240–246PubMedGoogle Scholar
  59. 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–R188Google Scholar
  60. 60.
    Kubis HP, Hanke N, Scheibe RJ, Meissner JD, Gros G (2003) Ca2+ transients activate calcineurin/NFATc1 and initiate fast-to-slow transformation in a primary skeletal muscle culture. Am J Physiol 285:C56–C63Google Scholar
  61. 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 35:27–31PubMedGoogle Scholar
  62. 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 277:46493–46503PubMedGoogle Scholar
  63. 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 472:595–614PubMedGoogle Scholar
  64. 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 418:797–801PubMedGoogle Scholar
  65. 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 155:27–39PubMedGoogle Scholar
  66. 66.
    Long YC, Widegren U, Zierath JR (2004) Exercise-induced mitogen-activated protein kinase signalling in skeletal muscle. Proc Nutr Soc 63:227–232PubMedGoogle Scholar
  67. 67.
    Market CL (1962) Lactate dehydrogenase isozymes: dissociation and recombination of subunits. Science 140:1329–1330Google Scholar
  68. 68.
    Martineau LC, Gardiner PF (2001) Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91:693–702PubMedGoogle Scholar
  69. 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:e288PubMedGoogle Scholar
  70. 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–E150PubMedGoogle Scholar
  71. 71.
    McGee SL, Hargreaves M (2004) Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes 53:1208–1214PubMedGoogle Scholar
  72. 72.
    McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27:40–47PubMedGoogle Scholar
  73. 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 97:14400–14405PubMedGoogle Scholar
  74. 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–E816PubMedGoogle Scholar
  75. 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 98:3820–3825PubMedGoogle Scholar
  76. 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 31:847–855PubMedGoogle Scholar
  77. 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 2:142–147PubMedGoogle Scholar
  78. 78.
    Nader GA, Esser KA (2001) Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol 90:1936–1942PubMedGoogle Scholar
  79. 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 275:4545–4548PubMedGoogle Scholar
  80. 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 312:1147–1153PubMedGoogle Scholar
  81. 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 96:189–194PubMedGoogle Scholar
  82. 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–R419Google Scholar
  83. 83.
    Ozawa K, Kondo T, Hori O, Kitao Y, Stern 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 108:41–50PubMedGoogle Scholar
  84. 84.
    Parry DJ (2001) Myosin heavy chain expression and plasticity: role of myoblast diversity. Exerc Sport Sci Rev 29:175–179PubMedGoogle Scholar
  85. 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 23:4331–4343PubMedGoogle Scholar
  86. 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 22:153–183PubMedGoogle Scholar
  87. 87.
    Pette D (1998) Training effects on the contractile apparatus. Acta Physiol Scand 162:367–376PubMedGoogle Scholar
  88. 88.
    Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types and transitions. Microsc Res Tech 50:500–509PubMedGoogle Scholar
  89. 89.
    Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202PubMedCrossRefGoogle Scholar
  90. 90.
    Pette D, Vrbova G (1999) What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve 22:666–667PubMedGoogle Scholar
  91. 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–E462PubMedGoogle Scholar
  92. 92.
    Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC1α gene in human skeletal muscle. J Physiol 546:851–858PubMedGoogle Scholar
  93. 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 92:829–839PubMedGoogle Scholar
  94. 94.
    Rao A, Luo C, Hogan PG (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707–747PubMedGoogle Scholar
  95. 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 111:277–287PubMedGoogle Scholar
  96. 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 4:253–260PubMedGoogle Scholar
  97. 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 275:8719–8725PubMedGoogle Scholar
  98. 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 52:2874–2881PubMedGoogle Scholar
  99. 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 278:44298–44304PubMedGoogle Scholar
  100. 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 275:1457–1462PubMedGoogle Scholar
  101. 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 224:215–225PubMedGoogle Scholar
  102. 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 28:324–329PubMedGoogle Scholar
  103. 103.
    Scarpulla RC (2002) Transcriptional activators and co-activators in the nuclear control of mitochondrial function in mammalian cells. Gene 286:81–89PubMedGoogle Scholar
  104. 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 131:147–154PubMedCrossRefGoogle Scholar
  105. 105.
    Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Phys Rev 76:371–423Google Scholar
  106. 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 15:148–157PubMedGoogle Scholar
  107. 107.
    Semenza GL (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19:176–182PubMedGoogle Scholar
  108. 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 271:32529–32537PubMedGoogle Scholar
  109. 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 98:13108–13113PubMedGoogle Scholar
  110. 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 97:277–285PubMedGoogle Scholar
  111. 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–C1728PubMedGoogle Scholar
  112. 112.
    Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424PubMedGoogle Scholar
  113. 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–C924Google Scholar
  114. 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 5:28PubMedGoogle Scholar
  115. 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 296:350–354Google Scholar
  116. 116.
    Thelen MHM, Simonides WS, Muller A, Van hardeveld C (1998) Cross talk between transcriptional regulation by thyroid hormone and myogenin: new aspect of Ca2+-dependent expression of the fast-type sarcoplasmic reticulum Ca2+–ATPase. Biochem J 329:131–136PubMedGoogle Scholar
  117. 117.
    Thompson HS, Maynard EB, Morales ER, Scordilis SP (2003) Exercise-induced HSP27, HSP70 and MAPK responses in human skeletal muscle. Acta Physiol Scand 178:61–72PubMedGoogle Scholar
  118. 118.
    Ventura-Clapier R, Veksler V, Hoerter JA (1994) Myofibrillar creatine kinase and cardiac contraction. Mol Cell Biochem 133–134:125–144PubMedGoogle Scholar
  119. 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 214:157–161PubMedGoogle Scholar
  120. 120.
    Wagner PD (2000) Diffusive resistance to O2 transport in muscle. Acta Physiol Scand 168:609–614PubMedGoogle Scholar
  121. 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 21:647–653PubMedGoogle Scholar
  122. 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):e294PubMedGoogle Scholar
  123. 123.
    Weis J, Kaussen M, Calvo S, Buonanno A (2000) Denervation induces a rapid nuclear accumulation of MRF4 in mature myofibers. Dev Dyn 218:438–451PubMedGoogle Scholar
  124. 124.
    Wenger RH (2002) Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene. FASEB J 16:1151–1162PubMedGoogle Scholar
  125. 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 12:1379–1389PubMedGoogle Scholar
  126. 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 510:623–632PubMedGoogle Scholar
  127. 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 88:2219–2226PubMedGoogle Scholar
  128. 128.
    Witmarsh AJ, Davis RJ (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74:589–607Google Scholar
  129. 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 535:155–164PubMedGoogle Scholar
  130. 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 98:115–124PubMedGoogle Scholar
  131. 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 19:1963–1973PubMedGoogle Scholar
  132. 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 20:414–6423Google Scholar
  133. 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 296:349–352PubMedGoogle Scholar
  134. 134.
    Yang SH, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320:3–21PubMedGoogle Scholar
  135. 135.
    York JW, Oscai LB, Penney DG (1974) Alterations in skeletal muscle lactate dehydrogenase isozymes following exercise training. Biochem Biophys Res Commun 61:1387–1393PubMedGoogle Scholar
  136. 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 536:273–282PubMedGoogle Scholar
  137. 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 546:327–335PubMedGoogle Scholar
  138. 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 19:21–30PubMedGoogle Scholar
  139. 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 194:186–193PubMedGoogle Scholar
  140. 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 543:191–200PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Département des Facteurs HumainsCentre de Recherches du Service de Santé des ArméesLa Tronche cedexFrance

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