Skip to main content
Log in

Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

The primary purpose of this study was to determine the relationship between myosin heavy chain (MHC) and actin contents and maximum isometric tetanic force (Po) in mouse extensor digitorum longus (EDL) muscles following eccentric contraction-induced injury. Po and protein contents were measured in injured (n=80) and contralateral control (n = 80) EDL muscles at the following time points after in vivo injury: sham, 0, 0.25, 1, 3, 5, 14, and 28 days. Po was reduced by 37 ± 2.3% to 49 ± 3.8% (p ≤ 0.05), while MHC and actin contents were unaltered from 0 to 3 days after injury. Whereas Po partially recovered between 3 and 5 days (from −49 ± 3.8% to −35 ± 3.6%), MHC and actin contents in the injured muscles declined by 19 ± 4.9% and 20 ± 5.3%, respectively, by 5 days compared with control muscles. Decrements in Po were similar to the reductions in MHC and actin contents at 14 (∼24%) and 28 (∼11%) days. Evaluation of myofibrillar and soluble protein fractions indicated significant reductions in the content of major proteins at 5 and 14 days. Immunoblots of heat shock protein 72 revealed elevations starting at 0.25 days, peaking during 1–3 days, and declining after 5days. These findings indicate that decreased contractile protein content is not related to the initial decrease in Po. However, decreased MHC and actin contents could account for 58% of the Po reduction at 5 days, and for nearly all the decrements in Po from 14 to 28 days.

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

  • Anathan, J., Goldberg, A. L. & Voellmy, R. (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232, 522–4.

    Google Scholar 

  • Armstrong, R. B., Ogilvie, R. W. & Schwane, J. A. (1983) Eccentric exercise-induced injury to rat skeletal muscle. J. Appl. Physiol. 54, 80–93.

    PubMed  CAS  Google Scholar 

  • Balnave, C. D. & Allen, D. G. (1995) Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J. Physiol. Lond. 488, 25–36.

    PubMed  CAS  Google Scholar 

  • Beckman, R. P., Mizzen, L. A. & Welch, W. J. (1990) Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 248, 850–54.

    Google Scholar 

  • Belcastro, A. N. (1993) Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J. Appl. Physiol. 74, 1381–6.

    PubMed  CAS  Google Scholar 

  • Bornman, L., Polla, B. S., Lotz, B. P. & Gericke, G. S. (1995) Expression of heat-shock/stress proteins in duchenne muscular dystrophy. Muscle and Nerve 18, 23–31.

    Article  PubMed  CAS  Google Scholar 

  • Brooks, S. V. & Faulkner, J. A. (1990) Isometric, shortening, and lengthening contractions of muscle fiber segments from adult and old mice. Am. J. Physiol. 267, C507–13.

    Google Scholar 

  • Close, R. I. (1972) Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52, 129–97.

    PubMed  CAS  Google Scholar 

  • Doherty, F. J. & Mayer, R. J. (1992) The mechanismspathways of intracellular proteolysis. In Intracellular Protein Degradation (edited by Rickwood, D. & Male, D.) pp. 15–32. New York: Oxford University Press.

    Google Scholar 

  • Evans, W. J., Meredith, C. N., Cannon, J. G., Dinarello, C. A., Frontera, W. R., Hughes, W. A., Jones, B. H. & Knuttgen, H. G. (1986) Metabolic changes following eccentric exercise in trained and untrained men. J. Appl. Physiol. 61, 1864–8.

    PubMed  CAS  Google Scholar 

  • Everett, A. W., Prior, G., Clark, W. A. & Zak, R. (1983) Quantitation of myosin in muscle. Anal. Biochem. 30, 102–7.

    Article  Google Scholar 

  • Fielding, R. A., Meredith, C. N., O'Reilly, K. P., Frontera, W. R., Cannon, J. G. & Evans, W. J. (1991) Enhanced protein breakdown after eccentric exercise in young and older men. J. Appl. Physiol. 71, 674–9.

    PubMed  CAS  Google Scholar 

  • FridÉn, J., Seger, J., SjÖstrÖm, M. & Ekblom, B. (1983) Adaptive response in human skeletal muscle subjected to prolonged eccentric training. Int. J. Sports Med. 4, 177–83.

    Article  PubMed  Google Scholar 

  • Goldberg, A. & Rock, K. (1992) Proteolysis, proteosomes and antigen presentation. Nature 357, 375–9.

    Article  PubMed  CAS  Google Scholar 

  • Goldberg, A. & St John, A. (1976) Intracellular protein degradation in mammalian and bacterial cells. Ann. Rev. Biochem. 45, 747–803.

    Article  PubMed  CAS  Google Scholar 

  • Ingalls, C. P., Warren, G. L., Lowe, D. A., Boorstein, D. B. & Armstrong, R. B. (1996) Differential effects of anesthetics on in vivo skeletal muscle contractile function in the mouse. J. Appl. Physiol. 80, 332–40.

    PubMed  CAS  Google Scholar 

  • Kantengwa, S., Capponi, A. M., Bonventre, J. V. & Polla, B. S. (1990) Calcium and the heat shock response in the human monocytic line U-937. Am. J. Physiol. 259, C77–83.

    PubMed  CAS  Google Scholar 

  • Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–85.

    Article  PubMed  CAS  Google Scholar 

  • Lowe, D. A., Warren, G. L., Hayes, D. A., Farmer, M. A. & Armstrong, R. B. (1994) Eccentric contractioninduced injury of mouse soleus muscle: effect of varying [Ca2+]o. J. Appl. Physiol. 76, 1445–53.

    PubMed  CAS  Google Scholar 

  • Lowe, D. A., Warren, G. L., Ingalls, C. P., Boorstein, D. B. & Armstrong, R. B. (1995) Muscle function and protein metabolism after initiation of eccentric contraction-induced injury. J. Appl. Physiol. 79, 1260–70.

    PubMed  CAS  Google Scholar 

  • Mair, J., Koller, A., Artner-Dworzak, E., Haid, C., Wicke, K., Judmaier, W. & Puschendoef, B. (1992) Effects of exercise on plasma heavy chain fragments and MRI of skeletal muscle. J. Appl. Physiol. 72, 656–63.

    PubMed  CAS  Google Scholar 

  • Mair, J., Mayr, M., Muller, E., Koller, A., Haid, C., Artner-Dworzak, E., Calzolari, C., Larue, C. M. & Puschendoef, B. (1995) Rapid adaptation to eccentric exercise-induced muscle damage. Int. J. Sports Med. 16, 352–6.

    PubMed  CAS  Google Scholar 

  • Mccully, K. K. & Faulkner, J. A. (1985) Injury to skeletal muscle fibers of mice following lengthening contractions. J. Appl. Physiol. 59, 119–26.

    PubMed  CAS  Google Scholar 

  • Mccully, K. K. & Faulkner, J. A. (1986) Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J. Appl. Physiol. 61, 293–9.

    PubMed  CAS  Google Scholar 

  • Morimoto, K. & Harrington, W. F. (1974) Substructure of the thick filament of vertebrate striated muscle. J. Mol. Biol. 83, 83–97.

    Article  PubMed  CAS  Google Scholar 

  • Newham, D. J., Mcphail, G., Mills, K. R. & Edwards, R. H. T. (1983) Ultrastructural changes after concentric and eccentric muscle contractions of human muscle. J. Neurol. Sci. 61, 109–22.

    Article  PubMed  CAS  Google Scholar 

  • Ogilvie, R. W., Armstrong, R. B., Baird, K. E. & Bottoms, C. L. (1988) Lesions in the rat soleus muscle following eccentrically biased exercise. Am. J. Anat. 182, 335–46.

    Article  PubMed  CAS  Google Scholar 

  • Raboy, B., Sharon, G., Parag, H. A., Shocat, Y. & Kulka, R. G. (1991) Effect of stress on protein degradation: role of the ubiquitin system. Acta Biol. Hung. 42, 3–20.

    PubMed  CAS  Google Scholar 

  • Rechsteiner, M. (1987) Ubiquitin-mediated pathways for intracellular proteolysis. Ann. Rev. Cell Biol. 3, 1–30.

    PubMed  CAS  Google Scholar 

  • Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, H. & Goldberg, A. L. (1994) Inhibitors of the proteosome block the degradation of most cell proteins and the generation of peptides presented on MHC Class I molecules. Cell 78, 761–71.

    Article  PubMed  CAS  Google Scholar 

  • Solaro, R. J., Pang, D. C. & Briggs, F. N. (1971) The purification of cardiac myofibrils with Triton X-100. Biochem. Biophys. Acta 245, 259–62.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, J. A. & Kandarian, S. C. (1994) Advantage of normalizing force production to myofibrillar protein in skeletal muscle cross-sectional area. J. Appl. Physiol. 76, 974–8.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, H. S. & Scordilis, S. P. (1994) Ubiquitin changes in human biceps muscle following exerciseinduced damage. Biochem. Biophys. Res. Comm. 204, 1193–8.

    Article  PubMed  CAS  Google Scholar 

  • Towbin, H., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA 76, 4350–54.

    Article  PubMed  CAS  Google Scholar 

  • Tsika, R. W., Herrick, R. E. & Baldwin, K. M. (1987) Time course adaptations in rat skeletal muscle isomyosins during compensatory growth and regression. J. Appl. Physiol. 63, 2111–21.

    PubMed  CAS  Google Scholar 

  • van Remmen, H., Ward, W. F., Sabia, R. V. & Richardson, A. (1995) Gene expression and protein degradation. In Handbook of Physiology-Aging (edited by MASORO, E. J.) pp. 211–34. New York: Oxford University Press.

    Google Scholar 

  • Warren, G. L., Hayes, D. A., Lowe, D. A., Williams, J. H. & Armstrong, R. B. (1994) Eccentric contractioninduced injury in normal and hindlimb-suspended mouse soleus and EDL muscles. J. Appl. Physiol. 77, 1421–30.

    PubMed  CAS  Google Scholar 

  • Warren, G. L., Lowe, D. A., Hayes, D.A., Farmer, M. A. & Armstrong, R. B. (1995) Redistribution of cell membrane probes following contraction-induced injury of mouse soleus muscle. Cell Tissue Res. 282, 311–20.

    PubMed  CAS  Google Scholar 

  • Warren, G. L., Lowe, D. A., Hayes, D. A., Karwoski, C. J., Prior, B. M. & Armstrong, R. B. (1993) Excitation failure in eccentric contraction-induced injury of mouse soleus muscle. J. Physiol. Lond. 468, 487–99.

    PubMed  CAS  Google Scholar 

  • Warren, G. L., Lowe, D. A., Inman, C. L., Orr, O. M., Hogan, H. A., Bloomfield, S. A., & Armstrong, R. B. (1996) Estradiol effects on anterior crural muscles: tibial bone relationship and susceptibility to injury. J. Appl. Physiol. 80, 1660–65.

    PubMed  CAS  Google Scholar 

  • Yates, L. D. & Greaser, M. L. (1983) Quantitative determination of myosin and actin in rabbit skeletal muscle. J. Mol. Biol. 168, 123–41.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ingalls, C.P., Warren, G.L. & Armstrong, R.B. Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 19, 215–224 (1998). https://doi.org/10.1023/A:1005368831198

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005368831198

Keywords

Navigation