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Journal of Muscle Research and Cell Motility

, Volume 40, Issue 3–4, pp 343–351 | Cite as

Skeletal muscle fibre swelling contributes to force depression in rats and humans: a mechanically-skinned fibre study

  • Daiki WatanabeEmail author
  • Travis L. Dutka
  • Cedric R. Lamboley
  • Graham D. Lamb
Original Article

Abstract

This study investigated the effects of fibre swelling on force production in rat and human skinned muscle fibres, using osmotic compression to reverse the fibre swelling. In mechanically-skinned fibres, the sarcolemma is removed but normal excitation–contraction coupling remains functional. Force responses in mechanically-skinned fibres were examined with and without osmotic compression by polyvinylpyrrolidone 40 kDa (PVP-40) or Dextran 500 kDa (dextran). Fibre diameter increased to 116 ± 2% (mean ± SEM) when rat skinned type II fibres were immersed in the standard intracellular solution, but remained close to the in situ size when 3% (mass/volume) PVP-40 or 4% Dextran were present. Myofibrillar Ca2+ sensitivity, as indicated by pCa50 (− log10[Ca2+] at half-maximal force), was increased in 4% Dextran (0.072 ± 0.007 pCa50 shift), but was not significantly changed in 3% PVP-40. Maximum Ca2+-activated force increased slightly to 103 ± 1% and 104 ± 1% in PVP-40 and Dextran, respectively. Both tetanic and depolarization-induced force responses in rat skinned type II fibres, elicited by electrical stimulation and ion substitution respectively, were increased by ~ 10 to 15% when the fibres were returned to their normal in situ diameter by addition of PVP-40 or Dextran. Interestingly, the potentiation of these force responses in PVP-40 was appreciably greater than could be explained by potentiation of myofibrillar function alone. These results indicate that muscle fibre swelling, as can occur with intense exercise, decreases evoked force responses by reducing both the Ca2+-sensitivity of the contractile apparatus properties and Ca2+ release from the sarcoplasmic reticulum.

Keywords

Osmolality Muscle swelling Excitation–contraction coupling Skinned fibre 

Notes

Acknowledgements

We thank Ms Maria Cellini for her technical assistance and the National Health and Medical Research Council of Australia (to G. D. Lamb, Grant No. 1085331) and Japan Society for the Promotion of Science (to D. Watanabe, Grant No. 16J01194) for financial support.

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Daiki Watanabe
    • 1
    • 2
    Email author
  • Travis L. Dutka
    • 1
  • Cedric R. Lamboley
    • 1
    • 3
  • Graham D. Lamb
    • 1
  1. 1.Department of Physiology Anatomy & MicrobiologyLa Trobe UniversityMelbourneAustralia
  2. 2.Graduate School of Integrated Arts and SciencesHiroshima UniversityHiroshimaJapan
  3. 3.School of Biomedical SciencesThe University of QueenslandBrisbaneAustralia

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