Skip to main content
Top
Published in: European Journal of Applied Physiology 7/2011

01-07-2011 | Original Article

Eccentric stimulation reveals an involvement of FGF6 in muscle resistance to mechanical stress

Authors: Iman Laziz, Arnaud Ferry, Anne-Sophie Armand, Claude Louis Gallien, Bruno Della Gaspera, F. Charbonnier, C. Chanoine

Published in: European Journal of Applied Physiology | Issue 7/2011

Login to get access

Abstract

The objective of this report was to analyse a potential role for FGF6 in muscle resistance to mechanical stress. Normal or regenerating muscles of FGF6 (−/−) mice versus wild-type mice were submitted to different protocols of damaging eccentric contractions (eccentric electrostimulation and intermittent downhill exercise). Then muscular structural properties were analysed by histological and immunochemistry techniques to evaluate the post-injury muscle recovery; their muscle contractile parameters (maximal tetanic force, kinetics properties and fatigue resistance) were assessed. The absence of FGF6 causes (1) a fast-to-slow myofibre type switch in adult control and regenerating Tibialis anterior (TA) muscle; (2) muscle weakness in regenerating muscles in animals submitted to eccentric exercise protocols due to aberrant extensive necrotic zones. These observations point out a crucial and unexpected role for FGF6 in muscle integrity and muscle protection against mechanical stress.
Literature
go back to reference Amali AA, Lin CJ, Chen YH, Wang WL, Gong HY, Rekha RD, Lu JK, Chen TT, Wu JL (2008) Overexpression of Myostatin2 in zebrafish reduces the expression of dystrophin associated protein complex (DAPC) which leads to muscle dystrophy. J Biomed Sci 15:595–604PubMedCrossRef Amali AA, Lin CJ, Chen YH, Wang WL, Gong HY, Rekha RD, Lu JK, Chen TT, Wu JL (2008) Overexpression of Myostatin2 in zebrafish reduces the expression of dystrophin associated protein complex (DAPC) which leads to muscle dystrophy. J Biomed Sci 15:595–604PubMedCrossRef
go back to reference Armand AS, Launay T, Gaspera BD, Charbonnier F, Gallien CL, Chanoine C (2003) Effects of eccentric treadmill running on mouse soleus: degeneration/regeneration studied with Myf-5 and MyoD probes. Acta Physiol Scand 179:75–84PubMedCrossRef Armand AS, Launay T, Gaspera BD, Charbonnier F, Gallien CL, Chanoine C (2003) Effects of eccentric treadmill running on mouse soleus: degeneration/regeneration studied with Myf-5 and MyoD probes. Acta Physiol Scand 179:75–84PubMedCrossRef
go back to reference Armand AS, Lécolle S, Launay T, Pariset C, Fiore F, Della Gaspera B, Birnbaum D, Chanoine C, Charbonnier F (2004) IGF-II is up-regulated and myofibres are hypertrophied in regenerating soleus of mice lacking FGF6. Exp Cell Res 297:27–38PubMedCrossRef Armand AS, Lécolle S, Launay T, Pariset C, Fiore F, Della Gaspera B, Birnbaum D, Chanoine C, Charbonnier F (2004) IGF-II is up-regulated and myofibres are hypertrophied in regenerating soleus of mice lacking FGF6. Exp Cell Res 297:27–38PubMedCrossRef
go back to reference Armand AS, Pariset C, Laziz I, Launay T, Fiore F, Della Gaspera B, Birnbaum D, Charbonnier F, Chanoine C (2005) FGF6 regulates muscle differentiation through a calcineurin-dependent pathway in regenerating soleus of adult mice. J Cell Physiol 204:297–308PubMedCrossRef Armand AS, Pariset C, Laziz I, Launay T, Fiore F, Della Gaspera B, Birnbaum D, Charbonnier F, Chanoine C (2005) FGF6 regulates muscle differentiation through a calcineurin-dependent pathway in regenerating soleus of adult mice. J Cell Physiol 204:297–308PubMedCrossRef
go back to reference Blair SN, Kohl HW, Barlow CE, Paffenbarger RS Jr, Gibbons LW, Macera CA (1995) Changes in physical fitness and all-cause mortality. A prospective study of healthy and unhealthy men. JAMA 14:1093–1098CrossRef Blair SN, Kohl HW, Barlow CE, Paffenbarger RS Jr, Gibbons LW, Macera CA (1995) Changes in physical fitness and all-cause mortality. A prospective study of healthy and unhealthy men. JAMA 14:1093–1098CrossRef
go back to reference Carter GT, Kikuchi N, Abresch RT, Walsh SA, Horasek SJ, Fowler WM (1994) Effects of exhaustive concentric and eccentric exercise on murine skeletal muscle. Arch Phys Med Rehabil 75:555–559PubMed Carter GT, Kikuchi N, Abresch RT, Walsh SA, Horasek SJ, Fowler WM (1994) Effects of exhaustive concentric and eccentric exercise on murine skeletal muscle. Arch Phys Med Rehabil 75:555–559PubMed
go back to reference Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159PubMedCrossRef Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159PubMedCrossRef
go back to reference Collins CA, Morgan JE (2003) Duchenne’s muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies. Int J Exp Pathol 84:165–172PubMedCrossRef Collins CA, Morgan JE (2003) Duchenne’s muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies. Int J Exp Pathol 84:165–172PubMedCrossRef
go back to reference Couteaux R, Mira JC, d’Albis A (1988) Regeneration of muscles after cardiotoxin injury I. Cytological aspects. Biol Cell 62:171–182PubMedCrossRef Couteaux R, Mira JC, d’Albis A (1988) Regeneration of muscles after cardiotoxin injury I. Cytological aspects. Biol Cell 62:171–182PubMedCrossRef
go back to reference Darr KC, Schultz E (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63:1816–1821PubMed Darr KC, Schultz E (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63:1816–1821PubMed
go back to reference Decraene C, Benchaouir R, Dillies MA, Israeli D, Bortoli S, Rochon C, Rameau P, Pitaval A, Tronik-Le Roux D, Danos O, Gidrol X, Garcia L, Pietu G (2005) Global transcriptional characterization of SP and MP cells from the myogenic C2C12 cell line: effect of FGF6. Physiol Genomics 23:132–149PubMedCrossRef Decraene C, Benchaouir R, Dillies MA, Israeli D, Bortoli S, Rochon C, Rameau P, Pitaval A, Tronik-Le Roux D, Danos O, Gidrol X, Garcia L, Pietu G (2005) Global transcriptional characterization of SP and MP cells from the myogenic C2C12 cell line: effect of FGF6. Physiol Genomics 23:132–149PubMedCrossRef
go back to reference Fielding RA, Violan MA, Svetkey L et al (2000) Effects of prior exercise on eccentric exercise-induced neutrophilia enzyme release. Med Sci Sports Exerc 32:359–364PubMedCrossRef Fielding RA, Violan MA, Svetkey L et al (2000) Effects of prior exercise on eccentric exercise-induced neutrophilia enzyme release. Med Sci Sports Exerc 32:359–364PubMedCrossRef
go back to reference Fiore F, Sébille A, Birnbaum D (2000) Skeletal muscle regeneration is not impaired in Fgf6 −/− mutant mice. Biochem Biophys Res Commum 272:138–143CrossRef Fiore F, Sébille A, Birnbaum D (2000) Skeletal muscle regeneration is not impaired in Fgf6 −/− mutant mice. Biochem Biophys Res Commum 272:138–143CrossRef
go back to reference Friden J, Lieber RL (2001) Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand 171:321–326PubMedCrossRef Friden J, Lieber RL (2001) Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand 171:321–326PubMedCrossRef
go back to reference Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176PubMedCrossRef Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176PubMedCrossRef
go back to reference Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729–738PubMedCrossRef Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729–738PubMedCrossRef
go back to reference Hikida RS, Staron RS, Hagerman FC, Sherman WM, Costill DL (1983) Muscle fiber necrosis associated with human marathon runners. J Neur Sci 59:185–203CrossRef Hikida RS, Staron RS, Hagerman FC, Sherman WM, Costill DL (1983) Muscle fiber necrosis associated with human marathon runners. J Neur Sci 59:185–203CrossRef
go back to reference Hosaka Y, Yokota T, Miyagoe-Suzuki Y, Yuasa K, Imamura M, Matsuda R, Ikemoto T, Kameya S, Takeda S (2002) Alpha1-syntrophin-deficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration. J Cell Biol 158:1097–1107PubMedCrossRef Hosaka Y, Yokota T, Miyagoe-Suzuki Y, Yuasa K, Imamura M, Matsuda R, Ikemoto T, Kameya S, Takeda S (2002) Alpha1-syntrophin-deficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration. J Cell Biol 158:1097–1107PubMedCrossRef
go back to reference Israeli D, Benchaouir R, Ziaei S, Rameau P, Gruszczynski C, Peltekian E, Danos O, Garcia L (2004) FGF6 mediated expansion of a resident subset of cells with SP phenotype in the C2C12 myogenic line. J Cell Physiol 201:409–419PubMedCrossRef Israeli D, Benchaouir R, Ziaei S, Rameau P, Gruszczynski C, Peltekian E, Danos O, Garcia L (2004) FGF6 mediated expansion of a resident subset of cells with SP phenotype in the C2C12 myogenic line. J Cell Physiol 201:409–419PubMedCrossRef
go back to reference Launay T, Armand AS, Charbonnier F, Mira JC, Donsez E, Gallien CL, Chanoine C (2001) Expression and neural control of myogenic regulatory factor genes during regeneration of mouse soleus. J Histochem Cytochem 49:887–900PubMedCrossRef Launay T, Armand AS, Charbonnier F, Mira JC, Donsez E, Gallien CL, Chanoine C (2001) Expression and neural control of myogenic regulatory factor genes during regeneration of mouse soleus. J Histochem Cytochem 49:887–900PubMedCrossRef
go back to reference McBride TA, Stockert BW, Gorin FA, Carlsen RC (2000) Stretch-activated ion channels contribute to membrane depolymerisation after eccentric contractions. J Appl Physiol 88:91–101PubMed McBride TA, Stockert BW, Gorin FA, Carlsen RC (2000) Stretch-activated ion channels contribute to membrane depolymerisation after eccentric contractions. J Appl Physiol 88:91–101PubMed
go back to reference 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 275:4545–4548PubMedCrossRef 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 275:4545–4548PubMedCrossRef
go back to reference Neuhaus P, Oustanina S, Loch T, Kruger M, Bober E, Dono R, Zeller R, Braun T (2003) Reduced mobility of fibroblast growth factor (FGF)-deficient myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple-mutant mice. Mol Cell Biol 23:6037–6048PubMedCrossRef Neuhaus P, Oustanina S, Loch T, Kruger M, Bober E, Dono R, Zeller R, Braun T (2003) Reduced mobility of fibroblast growth factor (FGF)-deficient myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple-mutant mice. Mol Cell Biol 23:6037–6048PubMedCrossRef
go back to reference Rudnicki MA, Le Grand F, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323–331PubMedCrossRef Rudnicki MA, Le Grand F, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323–331PubMedCrossRef
go back to reference Seale P, Rudnicki MA (2000) A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol 218:115–124PubMedCrossRef Seale P, Rudnicki MA (2000) A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol 218:115–124PubMedCrossRef
go back to reference Sjöström M, Fridén J, Ekblom B (1987) Endurance, what is it? Muscle morphology after an extremely long distance run. Acta Physiol Scand 130:513–520PubMedCrossRef Sjöström M, Fridén J, Ekblom B (1987) Endurance, what is it? Muscle morphology after an extremely long distance run. Acta Physiol Scand 130:513–520PubMedCrossRef
go back to reference Smith HK, Maxwell L, Rodgers CD, McKee NH, Plyley MJ (2001) Exercise-enhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 90:1407–1414PubMedCrossRef Smith HK, Maxwell L, Rodgers CD, McKee NH, Plyley MJ (2001) Exercise-enhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J Appl Physiol 90:1407–1414PubMedCrossRef
Metadata
Title
Eccentric stimulation reveals an involvement of FGF6 in muscle resistance to mechanical stress
Authors
Iman Laziz
Arnaud Ferry
Anne-Sophie Armand
Claude Louis Gallien
Bruno Della Gaspera
F. Charbonnier
C. Chanoine
Publication date
01-07-2011
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 7/2011
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-010-1784-0

Other articles of this Issue 7/2011

European Journal of Applied Physiology 7/2011 Go to the issue