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Differential effects of a six-day immobilization on newborn rat soleus muscles at two developmental stages

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Abstract

Our objective was to determine the effects of a six-day immobilization on the musculoskeletal system of the rat during postnatal development at two key periods when the states of innervation are known to be different. This work was undertaken on the soleus muscle since it is well known that postural slow muscles show marked changes after a period of disuse. Thus, the soleus muscle was immobilized in a shortened position either when the innervation was polyneuronal or monosynaptic, respectively from 6 to 12 and from 17 to 23 days. The muscle modifications were followed by ATPase staining and myosin heavy chain (MyHC) isoform identification using monoclonal antibodies and SDS–PAGE. The functional properties of skinned fibre bundles were established by calcium/strontium (Ca/Sr) activation characteristics. In control muscles the maturation was characterized by a progressive increase of adult MyHCs (I and IIA) concomitant with a decrease in both the MyHC neo and the Ca affinit y. Between 6 to 12 days, immobilization of the limb induced an increase in histochemical type IIC fibres. Using antibodies we identified new fibre types, classified as a function of their MyHC isoform co-expression. We observed an increase in expression of both MyHC neo and Ca affinity. From 17 to 23 days, the immobilization induced an increase in Ca affinity and marked changes in the MyHC isoform composition: disappearance of MyHC neo and expression of the fast MyHC IIB isoform, which in normal conditions is never expressed in the soleus muscle. We conclude that an immobilization imposed during polyneuronal innervation delays the postnatal maturation of the soleus muscle, whereas when the immobilization is performed under monosynaptic innervation the muscle evolves towards a fast phenotype using a default pathway for MyHC expression.

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References

  • ASMUSSEN, G. & SOUKUP, T. (1991) Arrest of developmental conversion of type II to type I fibres after suspension hypokinesia. Histochemical J. 23, 312–22.

    Google Scholar 

  • BAGUST, J., LEWIS, D. M. & WESTERMAN, R. A. (1973) Polyneuronal innervation of kitten skeletal muscle. J. Physiol. (London) 229, 241–55.

    Google Scholar 

  • BAKER, J. H. & MATSUMOTO, D. E. (1988) Adaptation of skeletal muscle to immobilization in a shortened position. Muscle & Nerve 11, 231–44.

    Google Scholar 

  • BENOIT, P. & CHANGEUX, J. P. (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Res. 99, 354–8.

    Google Scholar 

  • BRANDT, P. W., COX, R. N., KAWAI, M. & ROBINSON, T. (1982) Effect of cross-bridge kinetics on apparent Ca2+ sensitivity. J. Gen. Physiol. 79, 997–1016.

    Google Scholar 

  • BROWN, M. C., JANSEN, J. K. S. & VAN ESSEN, D. (1976) Polyneuronal innervation of skeletal muscle in newborn rats and its elimination during maturation. J. Physiol. (London) 261, 387–422.

    Google Scholar 

  • CARRARO, U. & CATANI, C. (1983) A sensitive SDS-PAGE method separating myosin heavy chain isoforms of rat skeletal muscles reveals the heterogeneous nature of the embryonic myosin. Biochem. Biophys. Res. Commun. 116, 793–802.

    Google Scholar 

  • CORDONNIER, C. (1994) Relation structure-fonction de fibres isoleées de muscles squelettiques. PhD thesis, Lille I University.

  • CORDONNIER, C., STEVENS, L., PICQUET, F. & MOUNIER, Y. (1995) Structure-function relationship of soleus muscle fibres from the rhesus monkey. Pflügers Arch. 430, 19–25.

    Google Scholar 

  • DANIELI-BETTO, D., BETTO, R. & MIDRIO, M. (1990) Calcium sensitivity and myofibrillar protein isoforms of rat skinned skeletal muscle fibres. Pflügers Arch. 417, 303–8.

    Google Scholar 

  • DANIELI-BETTO, D., ZERBATO, E. & BETTO, R. (1986) Type 1, 2A and 2B myosin heavy chain electrophoretic analysis of rat muscle fibres. Biochem. Biophys. Res. Commun. 138, 981–7.

    Google Scholar 

  • FABIATO, A. (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157, 378–417.

    Google Scholar 

  • FINK, R. H. A., STEPHENSON, D. G. & WILLIAMS, D. A. (1986) Calcium and strontium activation of single skinned muscle fibres of normal and dystrophic mice. J. Physiol. (London) 373, 513–25.

    Google Scholar 

  • FISHER, T. J., VRBOVA, G. & WIJETUNGE, A. (1989) Partial denervation of the rat soleus muscle at two different developmental stages. Neurosciences 28, 755–63.

    Google Scholar 

  • GAMBKE, B. & RUBINSTEIN, N. A. (1984) A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle. J. Biol. Chem. 259, 12092–100.

    Google Scholar 

  • GIULIAN, G. G., MOSS, R. L. & GREASER, M. L. (1983) Improved methodology for analysis and quantification of proteins on one dimensional silver stained slab gels. Anal. Biochem. 129, 277–87.

    Google Scholar 

  • GOLDSPINK, D. F. (1977) The influence of immobilization and stretch on protein turnover of rat skeletal muscle. J. Physiol. (London) 264, 267–82.

    Google Scholar 

  • GOLDSPINK, G., SCUTT, A., LOUGHNA, P. T., WELLS, D. J., JAENICKE, T. & GERLACH, G. F. (1992) Gene expression in skeletal muscle in response to stretch and force generation. Am. J. Physiol. 262, R356–63.

    Google Scholar 

  • GOLDSPINK, G. & WILLIAMS, P. E. (1989) The effects of immobilization on gene expression and post-natal determination of muscle fibre type in the mouse soleus muscle. J. Physiol. (London) 415, 52P.

    Google Scholar 

  • GUTH, L. & SAMAHA, F. J. (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. Exp. Neurol. 25, 138–52.

    Google Scholar 

  • HESLINGA, J. W. & HUIJING, P. A. (1992) Effect of short length immobilization of medial gastrocnemius muscle of growing young adult rats. Eur. J. Morph. 30, 257–73.

    Google Scholar 

  • HNIK, P., VEJSADA, R. & KASICKI, S. (1981) Reflex and locomotor changes following unilateral deafferentation of rat hindlimb assessed by chronic electromyography. Neurosciences 6, 195–203.

    Google Scholar 

  • JIANG, B., ROY, R. R. & EDGERTON, V. R. (1990) Expression of a fast fibre enzyme in the cat soleus after spinalization. Muscle & Nerve 13, 1038–49.

    Google Scholar 

  • KUGELBERG, E. (1976) Adaptive transformation of rat soleus motor units during growth. J. Neurological Sciences 27, 269–89.

    Google Scholar 

  • LEEUW, T., KAPP, M. & PETTE, D. (1994) Role of innervation for development and maintenance of troponin subunit isoform patterns in fast-and slow-twitch muscles of the rabbit. Differentiation 55, 193–201.

    Google Scholar 

  • LOUGHNA, P. T., ISUMO, S., GOLDSPINK, G. & NADAL-GINARD, B. (1990) Rapid changes in sarcomeric myosin heavy chain gene and alpha-actin expression in response to disuse and stretch. Development 109, 217–23.

    Google Scholar 

  • LOWRIE, M. B., MORE, A. F. K. & VRBOVA, G. (1989) The effect of load on the phenotype of the developing rat soleus muscle. Pflügers Arch. 415, 204–8.

    Google Scholar 

  • MOISESCU, D. G. & THIELECZEK, R. (1979) Sarcomere length effects of the Sr2+ and Ca2+ activation curves in skinned frog muscle fibres. Biochem. Biophys. Acta 546, 64–76.

    Google Scholar 

  • MOUNIER, Y., HOLY, X. & STEVENS, L. (1989) Compared properties of the contractile system of skinned slow and fast rat muscle fibres. Pflügers Arch. 415, 136–41.

    Google Scholar 

  • NAVARRETE, R. & VRBOVA, G. (1983) Changes of activity patterns in slow and fast muscles during postnatal development. Dev. Brain Res. 8, 11–19.

    Google Scholar 

  • ORENTLICHER, M., BRANDT, P. W. & REUBEN, J. P. (1977) Regulation of tension in skinned muscle fibres: effect of high concentrations of Mg-ATP. Am. J. Physiol. 233, 127–34.

    Google Scholar 

  • ORENTLICHER, M., REUBEN, J. P., GRUNDFEST, H. & BRANDT, P. W. (1974) Calcium binding and tension development in detergent-treated muscle fibres. J. Gen. Physiol. 63, 168–86.

    Google Scholar 

  • PICQUET, F., STEVENS, L., BUTLER-BROWNE, G. S. & MOUNIER, Y. (1997) Contractile properties and myosin heavy chain composition of newborn rat soleus muscles at different stages of postnatal development. J. Muscle Res. Cell Motil. 18, 71–9.

    Google Scholar 

  • REISER, P. J., KASPER, C. E., GREASER, M. L. & MOSS, R. L. (1988) Functional significance of myosin transitions in single fibers of developing soleus muscle. Am. J. Physiol. 254, C605–13.

    Google Scholar 

  • SPECTOR, J. A., SIMARD, C. P., FOURNIER, M., STERNLICHT, E. & EDGERTON, V. R. (1982) Architectural alterations of rat hindlimb skeletal muscle immobilized at different lengths. Exp. Neurol. 76, 94–110.

    Google Scholar 

  • STEVENS, L., MOUNIER, Y. & HOLY, X. (1993) Functional adaptation of different rat skeletal muscles to weightlessness. Am. J. Physiol. 264, R770–76.

    Google Scholar 

  • SZCZEPANOWSKA, J. & JAKUBIEC-PUKA, A. (1992) Myosin heavy chains in striated muscle after immobilization. Basic and Applied Myology 2, 97–105.

    Google Scholar 

  • TALMADGE, R. J. & ROY, R. R. (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 75, 2337–40.

    Google Scholar 

  • TERMIN, A., STARON, R. S. & PETTE, D. (1989) Myosin heavy chain isoforms in histochemically defined fiber types of rat muscle. Histochem. 92, 453–7.

    Google Scholar 

  • THOMASON, D. B. & BOOTH, F. W. (1990) Atrophy of the soleus muscle by hindlimb unweighting. J. Appl. Physiol. 68, 1–12.

    Google Scholar 

  • WESTERGA, J. & GRAMSBERGEN, A. (1994) Development of the EMG of the soleus muscle in the rat. Dev. Brain Res. 80, 233–43.

    Google Scholar 

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Picquet, F., Stevens, L., Butler-Browne, G.S. et al. Differential effects of a six-day immobilization on newborn rat soleus muscles at two developmental stages. J Muscle Res Cell Motil 19, 743–755 (1998). https://doi.org/10.1023/A:1005434917351

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