Skip to main content
Log in

The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

An animal suspension model has been used to simulate the weightlessness experienced during space travel. This procedure results in a reduction in the normal shortening (i.e. hypokinesia) and force generation functions of hind limb muscles (i.e. hypodynamia). The ensuing muscle atrophy was studied over 12 days in different muscle types. Slow muscles (e.g. the soleus) underwent a more pronounced atrophy than intermediate (i.e. gastrocnemius) and fast phasic muscles (e.g. extensor digitorum longus). In all muscle types inactivity resulted in a smaller accumulation of DNA and losses of RNA and protein after 5 days. The latter arose from a decrease in the rate of protein synthesis (measured in vivo) and an increase in protein breakdown. Increased specific activities of cathepsins B and D also supported the view that there is an increased proteolysis after hypokinesia and hypodynamia.

When the inactive soleus was simultaneously held in a lengthened (stretched) state the atrophy was prevented through a large increase in the fractional rate of protein synthesis. Protein degradation remained elevated with stretch, thereby slowing the growth of these muscles relative to those in pair-fed, ambulatory controls. The much smaller atrophy of the tibialis anterior and extensor digitorum longus muscles in suspended only limbs represented an underestimate of the true atrophic effects of hypokinesia and hypodynamia. In this model gravity pulls the suspended foot into a plantar flexed position, thereby permanently stretching and protecting such flexor muscles. When this influence of stretch was removed a greater atrophy ensued, mainly due to the loss of the stretch-induced stimulation of protein synthesis. Despite this, the inactive fast-twitch muscles still exhibited less atrophy than the gastrocnemius and soleus muscles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ariano MA, Armstrong RB, Edgerton VR (1973) Hindlimb muscle fibre populations of five mammals. J Histochem Cytochem 21:51–55

    Google Scholar 

  • Barrett AJ (1980) Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates. Biochem J 187:909–912

    Google Scholar 

  • Booth FW, Nicholson WF, Watson PA (1982) Exercise and sports science reviews, vol 10. Franklin Institute Press, Philadelphia, pp 27–48

    Google Scholar 

  • Chiu LA, Castleman KR (1980) Morphometric analysis of rat muscle fibres following space flight and hypogravity. Physiologist 23:S76-S78

    Google Scholar 

  • Feller DD, Ginoza HS, Morey ER (1981) Atrophy of rat skeletal muscles in simulated weightlessness. Physiologist 24:S9-S10

    Google Scholar 

  • Garlick PJ, Fern EB, McNurlan MA (1979) Methods for determining protein turnover. In: Rapoport S, Schewe T (eds) Processing and turnover of proteins and organelles in the cell, vol 53. Proc. FEBS. Pergamon Press, Oxford-New York, pp 85–94

    Google Scholar 

  • Garlick PJ, McNurlan MA, Preedy VR (1980) A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of (H)3 phenylalanine. Biochem J 192:719–723

    Google Scholar 

  • Goldberg AL, Goldspink, DF (1975) Influence of food deprivation and adrenal steroids on DNA synthesis in various mammalian tissues. Am J Physiol 228:310–317

    Google Scholar 

  • Goldspink DF (1977) The influence of immobilization and stretch and protein turnover of rat skeletal muscle. J Physiol 264:267–282

    Google Scholar 

  • Goldspink DF (1978) The influence of passive stretch on the growth and protein turnover of the denervated extensor digitorum longus muscle. Biochem J 174:595–602

    Google Scholar 

  • Goldspink DF (1980) Physiological factors influencing protein turnover and muscle growth in mammals. In: Goldspink DF (ed) The development and specialization of skeletal muscle. Cambridge University Press, pp 65–89

  • Goldspink DF, Lewis SEM (1985) Developmental changes and the influence of exercise, stretch and innervation on muscle growth. In: Glaumann H, Ballard FJ (eds) Lysosomes: Their role in protein breakdown. Academic Press (in press)

  • Goldspink DF, Lewis SEM, Kelly FJ (1985) Protein turnover and cathepsin B activity in several individual tissues of foetal and senescent rats. Comp Biochem Physiol 82 B, 849–853

    Google Scholar 

  • Goldspink G, Tabary JC, Tabary C, Tardieu G (1974) Effect of denervation on the adaptation of sarcomere number and muscle extensibility to the functional length of the muscle. J Physiol 236:733–742

    Google Scholar 

  • Holly RG, Barnett JG, Ashmore CR, Taylor RG, Mole PA (1980) Stretch-induced growth in chicken wing muscles: A new model of stretch hypertrophy. Am J Physiol 238:C62-C71

    Google Scholar 

  • Kazaryan VA, Rapoport EA, Goncharova LA, Bulychewa SY (1977) Effect of prolonged weightlessness on protein metabolism in red and white skeletal muscles of rats. Kosm Biol Aviakosm Med 11:19–23

    Google Scholar 

  • Loughna PT, Goldspink G, Goldspink DF (1986a) Protein turnover in phasic and postural hindlimb muscles of the rat in response to hypokinesia, hypodynamia and passive stretch. Am J Appl Physiol (in press)

  • Loughna PT, Cook P, Goldspink DF, Goldspink G (1986b) Muscle fibre atrophy during disuse and its prevention by passive stretch. Cell Tissue Res (in press)

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    Google Scholar 

  • Morey ER (1979) Spaceflight and bone-turnover-correlation with a new rat model of weightlessness. Bioscience 29:168–172

    Google Scholar 

  • Morey ER, Baylink DJ (1978) Inhibition of bone formation during space flight. Science 201:1138–1141

    Google Scholar 

  • Morey-Holton E, Wronski WJ (1981) Animal models for simulating weightlessness. Physiologist 24:S45-S48

    Google Scholar 

  • Musacchia XJ, Steffen JM, Deavers DR (1981) Suspension restraint: reduced hypokinesia antiorthostasis as a simulation of weightlessness. Physiologist 24:S21-S22

    Google Scholar 

  • Musacchia XJ, Deavers DR, Meininger G, Davis TP (1980) A model for hypokinesia: effects on muscle atrophy in the rat. J Appl Physiol 48:479–486

    Google Scholar 

  • Palmer RM, Reeds PJ, Atkinson T, Smith RH (1983) The influence of changes in tension on protein synthesis and prostaglandin release in isolated rabbit muscles. Biochem J 214:1011–1014

    Google Scholar 

  • Pennington RJT (1977) Proteinases of muscle. In: Barrett AJ (ed) Proteinases in mammalian cells and tissues. North Holland, Amsterdam, pp 515–543

    Google Scholar 

  • Pette D (ed) Plasticity of muscle. Walter de Gruyter, Berlin New York

  • Pluskal MG, Pennington RJ (1973) Peptide hydrolase activities in denervated muscle. Biochem Soc Trans 1:1307–1310

    Google Scholar 

  • Rodemann HP, Goldberg AL (1982) Arachidonic acid, prostaglandin E2 and F2 influence rates of protein turnover in sceletal and cardiac muscle. J Biol Chem 257:1632–1638

    Google Scholar 

  • Sargeant AJ, Davies LTM, Edwards RHT, Maunder C, Young A (1977) Functional and structural changes after disuse of human muscle. Clin Sci Mol Med 52:337–342

    Google Scholar 

  • Shear CR (1978) Cross sectional myofibre and myofibril growth in immobilized developing skeletal muscle. J Cell Sci 29:297–312

    Google Scholar 

  • Templeton GH, Padalino M, Manton J, Glasberg M, Silver CJ, Silver P, De Martino G, Leconey T, Klug G, Hagler H, Sutko JL (1984) Evaluation to the response of rat skeletal muscle to a model of weightlessness. Physiologist 25:S513-S514

    Google Scholar 

  • Tischler ME, Jaspers SR (1982) Synthesis of amino acids in weight bearing and non weight bearing leg muscles of suspended rats. Physiologist 25:S155-S156

    Google Scholar 

  • Waterlow JC, Garlick PJ, Millward DJ (eds) (1978) Protein turnover in mammalian tissues and in the whole body. North Holland, Amsterdam, pp 625–696

    Google Scholar 

  • Watson PA, Stein JP, Booth FW (1984) Changes in actin synthesis and actin-mRNA content in rat muscle during immobilization. Am J Physiol 247:C39-C44

    Google Scholar 

  • Williams PE, Goldspink G (1973) The effect of immobilization on the longitudinal growth of striated muscle. J Anat 116:45–55

    Google Scholar 

  • Williams PE, Goldspink G (1978) Changes in sarcomere length and physiological properties in immobilized muscle. J Anat 127:459–468

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goldspink, D.F., Morton, A.J., Loughna, P. et al. The effect of hypokinesia and hypodynamia on protein turnover and the growth of four skeletal muscles of the rat. Pflügers Arch. 407, 333–340 (1986). https://doi.org/10.1007/BF00585311

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00585311

Key words

Navigation