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. 1978 Aug 15;174(2):595–602. doi: 10.1042/bj1740595

The influence of passive stretch on the growth and protein turnover of the denervated extensor digitorum longus muscle

David F Goldspink 1
PMCID: PMC1185952  PMID: 708412

Abstract

At 7 days after cutting the sciatic nerve, the extensor digitorum longus muscle was smaller and contained less protein than its innervated control. Correlating with these changes was the finding of elevated rates of protein degradation (measured in vitro) in the denervated tissue. However, at this time, rates of protein synthesis (measured in vitro) and nucleic acid concentrations were also higher in the denervated tissue, changes more usually associated with an active muscle rather than a disused one. These anabolic trends have, at least in part, been explained by the possible greater exposure of the denervated extensor digitorum longus to passive stretch. When immobilized under a maintained influence of stretch the denervated muscle grew to a greater extent. Although this stretch-induced growth appeared to occur predominantly through a stimulation of protein synthesis, it was opposed by smaller increases in degradative rates. Nucleic acids increased at a similar rate to the increase in muscle mass when a continuous influence of stretch was imposed on the denervated tissue. In contrast, immobilization of the denervated extensor digitorum longus in a shortened unstretched state reversed most of the stretch-induced changes; that is, the muscle became even smaller, with protein synthesis decreasing to a greater extent than breakdown after the removal of passive stretch. The present investigation suggests that stretch will promote protein synthesis and hence growth of the extensor digitorum longus even in the absence of an intact nerve supply. However, some factor(s), in addition to passive stretch, must contribute to the anabolic trends in this denervated muscle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Buresová M., Gutmann E., Klicpera M. Effect of tension upon rate of incorporation of amino acids into proteins of cross-striated muscle. Experientia. 1969 Feb 15;25(2):144–145. doi: 10.1007/BF01899088. [DOI] [PubMed] [Google Scholar]
  2. Fulks R. M., Li J. B., Goldberg A. L. Effects of insulin, glucose, and amino acids on protein turnover in rat diaphragm. J Biol Chem. 1975 Jan 10;250(1):290–298. [PubMed] [Google Scholar]
  3. GUTMANN E., ZAK R. Nervous regulation of nucleic acid level in cross-striated muscle. Changes in denervated muscle. Physiol Bohemoslov. 1961;10:493–500. [PubMed] [Google Scholar]
  4. Goldberg A. L., Jablecki C., Li J. B. Trophic functions of the neuron. 3. Mechanisms of neurotrophic interactions. Effects of use and disuse on amino acid transport and protein turnover in muscle. Ann N Y Acad Sci. 1974 Mar 22;228(0):190–201. doi: 10.1111/j.1749-6632.1974.tb20510.x. [DOI] [PubMed] [Google Scholar]
  5. Goldberg A. L. Protein turnover in skeletal muscle. II. Effects of denervation and cortisone on protein catabolism in skeletal muscle. J Biol Chem. 1969 Jun 25;244(12):3223–3229. [PubMed] [Google Scholar]
  6. Goldspink D. F., Goldberg A. L. Problems in the use of (Me- 3H) thymidine for the measurement of DNA synthesis. Biochim Biophys Acta. 1973 Apr 11;299(4):521–532. doi: 10.1016/0005-2787(73)90224-4. [DOI] [PubMed] [Google Scholar]
  7. Goldspink D. F. The effects of denervation on protein turnover of rat skeletal muscle. Biochem J. 1976 Apr 15;156(1):71–80. doi: 10.1042/bj1560071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldspink D. F. The influence of activity on muscle size and protein turnover. J Physiol. 1977 Jan;264(1):283–296. doi: 10.1113/jphysiol.1977.sp011668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hamosch M., Lesch M., Baron J., Kaufman S. Enhanced protein synthesis in a cell-free system from hypertrophied skeletal muscle. Science. 1967 Aug 25;157(3791):935–937. doi: 10.1126/science.157.3791.935. [DOI] [PubMed] [Google Scholar]
  10. Harris E. J., Manchester K. L. The effects of potassium ions and denervation on protein synthesis and the transport of amino acids in muscle. Biochem J. 1966 Oct;101(1):135–145. doi: 10.1042/bj1010135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  12. Lewis D. M. Effect of denervation on the differentiation of twitch muscles in the kitten hind limb. Nat New Biol. 1973 Feb 28;241(113):285–286. doi: 10.1038/newbio241285a0. [DOI] [PubMed] [Google Scholar]
  13. Mallet L. E., Exton J. H., Park C. R. Control of gluconeogenesis from amino acids in the perfused rat liver. J Biol Chem. 1969 Oct 25;244(20):5713–5723. [PubMed] [Google Scholar]
  14. Manchester K. L., Harris E. J. Effect of denervation on the synthesis of ribonucleic acid and deoxyribonucleic acid in rat diaphragm muscle. Biochem J. 1968 Jun;108(2):177–183. doi: 10.1042/bj1080177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Millward D. J., Garlick P. J., James W. P., Nnanyelugo D. O., Ryatt J. S. Relationship between protein synthesis and RNA content in skeletal muscle. Nature. 1973 Jan 19;241(5386):204–205. doi: 10.1038/241204a0. [DOI] [PubMed] [Google Scholar]
  16. Muscatello U., Margreth A., Aloisi M. On the differential response of sarcoplasm and myoplasm to denervation in frog muscle. J Cell Biol. 1965 Oct;27(1):1–24. doi: 10.1083/jcb.27.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pater J. L., Kohn R. R. Turnover of structural protein fractions in denervated muscle. Proc Soc Exp Biol Med. 1967 Jun;125(2):476–481. doi: 10.3181/00379727-125-32124. [DOI] [PubMed] [Google Scholar]
  18. Peterson M. B., Lesch M. Protein synthesis and amino acid transport in the isolated rabbit right ventricular papillary muscle. Effect of isometric tension development. Circ Res. 1972 Sep;31(3):317–327. doi: 10.1161/01.res.31.3.317. [DOI] [PubMed] [Google Scholar]
  19. SOLA O. M., MARTIN A. W. Denervation hypertrophy and atrophy of the hemidiaphragm of the rat. Am J Physiol. 1953 Feb;172(2):324–332. doi: 10.1152/ajplegacy.1953.172.2.324. [DOI] [PubMed] [Google Scholar]
  20. Sola O. M., Christensen D. L., Martin A. W. Hypertrophy and hyperplasia of adult chicken anterior latissimus dorsi muscles following stretch with and without denervation. Exp Neurol. 1973 Oct;41(1):76–100. doi: 10.1016/0014-4886(73)90182-9. [DOI] [PubMed] [Google Scholar]
  21. Turner L. V., Garlick P. J. The effect of unilateral phrenicectomy on the rate of protein synthesis in rat diaphragm in vivo. Biochim Biophys Acta. 1974 Apr 27;349(1):109–113. doi: 10.1016/0005-2787(74)90013-6. [DOI] [PubMed] [Google Scholar]
  22. WAALKES T. P., UDENFRIEND S. A fluorometric method for the estimation of tyrosine in plasma and tissues. J Lab Clin Med. 1957 Nov;50(5):733–736. [PubMed] [Google Scholar]
  23. Williams P. E., Goldspink G. The effect of denervation and dystrophy on the adaptation of sarcomere number to the functional length of the muscle in young and adult mice. J Anat. 1976 Nov;122(Pt 2):455–465. [PMC free article] [PubMed] [Google Scholar]
  24. Williams P. E., Goldspink G. The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat. 1973 Oct;116(Pt 1):45–55. [PMC free article] [PubMed] [Google Scholar]

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