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TGF-β1 favors the development of fast type identity during soleus muscle regeneration

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Abstract

Transforming growth factor-β1 (TGF-β1) is known to be expressed in the environment of developing fast muscle fibres during ontogenesis. In the present study, we have examined effects of administration of either TGF-β1 or neutralizing TGF-β1 antibody on the induction of fast type phenotype in regenerating skeletal muscles in rats. Expressions of fast and slow myosin heavy chain (MHC) isoforms were studied using protein electrophoresis, at 3 and 6 weeks after myotoxic treatment. Muscle contractile properties were also measured in situ. The results have shown that a single injection of TGF-β1 into the regenerating slow soleus muscle increased the expression of fast MHC-2x/d and MHC-2a and decreases that of slow MHC-1 (P<0.05). Moreover, it reduced the degree of tetanic fusion during contraction (P<0.05). Conversely, injection of neutralizing antibody against TGF-β1 into the regenerating fast EDL muscle increased the expression of MHC-2a and MHC-1 (P<0.05). In conclusion, when the slow muscle was regenerating in the presence of an increased level of TGF-β1, it induced a shift to a less slow MHC phenotype and contractile characteristics. Conversely, neutralization of TGF-β1 in the regenerating fast muscle induced a shift to a less fast MHC expression. Together these results suggest that TGF-β1 influences some aspects of fast muscle-type patterning during skeletal muscle regeneration.

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References

  • Agbulut O, Li Z, Mouly V, Butler-Browne GS, (1996). Analysis of skeletal and cardiac muscle from desmin knock-out and normal mice by high resolution separation of myosin heavy-chain isoformsBiol Cell 88: 131–135

    Article  PubMed  CAS  Google Scholar 

  • Bren-Mattison Y, Olwin BB, (2002). Sonic hedgehog inhibits the terminal differentiation of limb myoblasts committed to the slow muscle lineageDev Biol 242: 130–148

    Article  PubMed  CAS  Google Scholar 

  • Calvo S, Vullhorst D, Venepally P, Cheng J, Karavanova I, Buonanno A, (2001). Molecular dissection of DNA sequences and factors involved in slow muscle-specific transcriptionMol Cell Biol 21: 8490–8503

    Article  PubMed  CAS  Google Scholar 

  • Carlson CJ, Booth FW, Gordon SE, (1999). Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloadingAm J Physiol 277: R601–R606

    PubMed  CAS  Google Scholar 

  • Caruelle D, Mazouzi Z, Husmann I, Delbe J, Duchesnay A, Gautron J, Martelly I, Courty J, (2004). Upregulation of HARP during in vitro myogenesis and rat soleus muscle regenerationJ Muscle Res Cell Motil 25: 45–53

    Article  PubMed  CAS  Google Scholar 

  • Cusella-De Angelis MG, Molinari S, Le Donne A, Coletta M, Vivarelli E, Bouche M, Molinaro M, Ferrari S, Cossu G, (1994). Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesisDevelopment 120: 925–933

    PubMed  CAS  Google Scholar 

  • d’Albis A, Couteaux R, Janmot C, Roulet A, Mira JC, (1988). Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals. Myosin isoform analysisEur J Biochem 174: 103–110

    Article  PubMed  CAS  Google Scholar 

  • De Angelis L, Borghi S, Melchionna R, Berghella L, Baccarani-Contri M, Parise F, Ferrari S, Cossu G, (1998). Inhibition of myogenesis by transforming growth factor beta is density-dependent and related to the translocation of transcription factor MEF2 to the cytoplasmProc Natl Acad Sci USA 95: 12358–12363

    Article  PubMed  Google Scholar 

  • Devor ST, White TP, (1996). Myosin heavy chain of immature soleus muscle grafts adapts to hyperthyroidism more than to physical activityJ Appl Physiol 80: 789–794

    PubMed  CAS  Google Scholar 

  • Duprez D, (2002). Signals regulating muscle formation in the limb during embryonic developmentInt J Dev Biol 46: 915–925

    PubMed  CAS  Google Scholar 

  • Esser K, Nelson T, Lupa-Kimball V, Blough E, (1999). The CACC box and myocyte enhancer factor-2 sites within the myosin light chain 2 slow promoter cooperate in regulating nerve-specific transcription in skeletal muscleJ Biol Chem 274: 12095–12102

    Article  PubMed  CAS  Google Scholar 

  • Fluck M, Hoppeler H, (2003). Molecular basis of skeletal muscle plasticity – from gene to form and functionRev Physiol Biochem Pharmacol 146: 159–216

    Article  PubMed  CAS  Google Scholar 

  • Gerrits HL, Hopman MT, Offringa C, Engelen BG, Sargeant AJ, Jones DA, Haan A, (2003). Variability in fibre properties in paralysed human quadriceps muscles and effects of trainingPflugers Arch 445: 734–740

    PubMed  CAS  Google Scholar 

  • Goetsch SC, Hawke TJ, Gallardo TD, Richardson JA, Garry DJ, (2003). Transcriptional profiling and regulation of the extracellular matrix during muscle regenerationPhysiol Genomics 14: 261–271

    PubMed  CAS  Google Scholar 

  • Grifone R, Laclef C, Spitz F, Lopez S, Demignon J, Guidotti JE, Kawakami K, Xu PX, Kelly R, Petrof BJ, Daegelen D, Concordet JP, Maire P, (2004). Six1 and Eya1 expression can reprogram adult muscle from the slow-twitch phenotype into the fast-twitch phenotypeMol Cell Biol 24: 6253–6267

    Article  PubMed  CAS  Google Scholar 

  • Harris JB, (2003). Myotoxic phospholipases A2 and the regeneration of skeletal musclesToxicon 42: 933–945

    Article  PubMed  CAS  Google Scholar 

  • Hughes SM, Blagden CS, Li X, Grimaldi A, (1998). The role of hedgehog proteins in vertebrate slow and fast skeletal muscle patterningActa Physiol Scand 163: S7–S10

    Article  PubMed  CAS  Google Scholar 

  • Hughes SM, Salinas PC, (1999). Control of muscle fibre and motoneuron diversificationCurr Opin Neurobiol 9: 54–64

    Article  PubMed  CAS  Google Scholar 

  • Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, Peterson CA, (1993). Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormonesDevelopment 118: 1137–1147

    PubMed  CAS  Google Scholar 

  • Husmann I, Soulet L, Gautron J, Martelly I, Barritault D, (1996). Growth factors in skeletal muscle regenerationCytokine Growth Factor Rev 7: 249–258

    Article  PubMed  CAS  Google Scholar 

  • Kalhovde JM, Jerkovic R, Sefland I, Cordonnier C, Calabria E, Schiaffino S, Lomo T, (2005). “Fast” and “slow” muscle fibres in hindlimb muscles of adult rats regenerate from intrinsically different satellite cellsJ Physiol 562: 847–857

    Article  PubMed  CAS  Google Scholar 

  • Lagord C, Soulet L, Bonavaud S, Bassaglia Y, Rey C, Barlovatz-Meimon G, Gautron J, Martelly I, (1998). Differential myogenicity of satellite cells isolated from extensor digitorum longus (EDL) and soleus rat muscles revealed in vitroCell Tissue Res 291: 455–468

    Article  PubMed  CAS  Google Scholar 

  • Lefaucheur JP, Sebille A, (1995). Muscle regeneration following injury can be modified in vivo by immune neutralization of basic fibroblast growth factor, transforming growth factor beta 1 or insulin-like growth factor IJ Neuroimmunol 57: 85–91

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Huard J, (2002). Differentiation of muscle-derived cells into myofibroblasts in injured skeletal muscleAm J Pathol 161: 895–907

    PubMed  Google Scholar 

  • McLennan IS, (1993). Localisation of transforming growth factor beta 1 in developing muscles: implications for connective tissue and fiber type pattern formationDev Dyn 197: 281–290

    PubMed  CAS  Google Scholar 

  • McLennan IS, Koishi K, (1997). Cellular localisation of transforming growth factor-beta 2 and -beta 3 (TGF-beta2, TGF-beta3) in damaged and regenerating skeletal musclesDev Dyn 208: 278–289

    Article  PubMed  CAS  Google Scholar 

  • Murgia M, Serrano AL, Calabria E, Pallafacchina G, Lomo T, Schiaffino S, (2000). Ras is involved in nerve-activity-dependent regulation of muscle genesNat Cell Biol 2: 142–147

    Article  PubMed  CAS  Google Scholar 

  • Noirez P, Agbulut O, Ferry A, (2000). Differential modification of myosin heavy chain expression by tenotomy in regenerating fast and slow muscles of the ratExp Physiol 85: 187–191

    Article  PubMed  CAS  Google Scholar 

  • Pin CL, Hrycyshyn AW, Rogers KA, Rushlow WJ, Merrifield PA, (2002). Embryonic and fetal rat myoblasts form different muscle fiber types in an ectopic in vivo environmentDev Dyn 224: 253–266

    Article  PubMed  Google Scholar 

  • Rosenblatt JD, Parry DJ, Partridge TA, (1996). Phenotype of adult mouse muscle myoblasts reflects their fiber type of originDifferentiation 60: 39–45

    Article  PubMed  CAS  Google Scholar 

  • Sakuma K, Watanabe K, Sano M, Kitajima S, Sakamoto K, Uramoto I, Totsuka T, (2000). The adaptive response of transforming growth factor-beta 2 and -beta RII in the overloaded, regenerating and denervated muscles of ratsActa Neuropathol (Berl) 99: 177–185

    Article  CAS  Google Scholar 

  • Schiaffino S, Reggiani C, (1996). Molecular diversity of myofibrillar proteins: gene regulation and functional significancePhysiol Rev 76: 371–423

    PubMed  CAS  Google Scholar 

  • Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lomo T, Schiaffino S, (2001). Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growthProc Natl Acad Sci USA 98: 13108–13113

    Article  PubMed  CAS  Google Scholar 

  • Snoj-Cvetko E, Sketelj J, Dolenc I, Obreza S, Janmot C, d’Albis A, Erzen I, (1996). Regenerated rat fast muscle transplanted to the slow muscle bed and innervated by the slow nerve, exhibits an identical myosin heavy chain repertoire to that of the slow muscleHistochem Cell Biol 106: 473–479

    Article  PubMed  CAS  Google Scholar 

  • Spangenburg EE, Booth FW, (2003). Molecular regulation of individual skeletal muscle fibre typesActa Physiol Scand 178: 413–424

    Article  PubMed  CAS  Google Scholar 

  • Vignaud A, Noirez P, Besse S, Rieu M, Barritault D, Ferry A, (2003). Recovery of slow skeletal muscle after injury in the senescent ratExp Gerontol 38: 529–537

    Article  PubMed  CAS  Google Scholar 

  • Vignaud A, Hourde C, Torres S, Caruelle JP, Martelly I, Keller A, Ferry A, (2005). Functional, cellular and molecular aspects of skeletal muscle recovery after injury induced by snake venom from notechis scutatus. Toxicon, 45 789–801

    Article  PubMed  CAS  Google Scholar 

  • Wehrle U, Dusterhoft S, Pette D, (1994). Effects of chronic electrical stimulation on myosin heavy chain expression in satellite cell cultures derived from rat muscles of different fiber-type compositionDifferentiation 58: 37–46

    Article  PubMed  CAS  Google Scholar 

  • Whalen RG, Harris JB, Butler-Browne GS, Sesodia S, (1990). Expression of myosin isoforms during notexin-induced regeneration of rat soleus musclesDev Biol 141: 24–40

    Article  PubMed  CAS  Google Scholar 

  • Wigmore PM, Evans DJ, (2002). Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesisInt Rev Cytol 216: 175–232

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K, Kuzon WM, Harii K, (1998). Myosin heavy chain expression in skeletal muscle autografts under neural or aneural conditionsJ Surg Res 75: 135–147

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Koishi K, McLennan IS (1998). Skeletal muscle fibre types: detection methods and embryonic determinantsHistol Histopathol 13: 201–207

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are very grateful to Thierry Launay (Laboratoire de Biologie du Développement et de la Différenciation Neuromusculaire, Paris), Michel Rieu, Imed Ben Salah (Laboratoire de Physiologie des Adaptations, Faculté de Médecine Cochin Port-Royal, Paris), Alban Vignaud and Nicolas Bardes (CNRS FRE 2412).

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Authors and Affiliations

  1. CNRS FRE 2412, Créteil, France

    Philippe Noirez, Sandra Torres, José Cebrian, Juliette Peltzer, Isabelle Martelly, Angelica Keller & Arnaud Ferry

  2. CNRS UMR 7000, Paris, France

    Philippe Noirez, Onnik Agbulut & Gillian Butler-Browne

  3. Université Paris 5, Paris, France

    Philippe Noirez

  4. INSERM U567-CNRS UMR 8104, Paris, France

    Dominique Daegelen

  5. Laboratoire CRRET, CNRS FRE 2412, Faculté de Sciences et Technologies, 61 avenue du Général de Gaulle, 94010, Créteil, France

    Arnaud Ferry

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  1. Philippe Noirez
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  2. Sandra Torres
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  3. José Cebrian
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  9. Angelica Keller
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  10. Arnaud Ferry
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Correspondence to Arnaud Ferry.

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Noirez, P., Torres, S., Cebrian, J. et al. TGF-β1 favors the development of fast type identity during soleus muscle regeneration. J Muscle Res Cell Motil 27, 1–8 (2006). https://doi.org/10.1007/s10974-005-9014-9

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  • DOI: https://doi.org/10.1007/s10974-005-9014-9

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