Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats

Krishnan S. Ramaswamy, Mark L. Palmer, Jack H. Van Der Meulen, Abigail Renoux, Tatiana Y. Kostrominova, Daniel E. Michele, John A. Faulkner

Research output: Contribution to journalArticle

113 Scopus citations

Abstract

The dystrophin-glycoprotein complex (DGC) provides an essential link from the muscle fibre cytoskeleton to the extracellular matrix. In dystrophic humans and mdx mice, mutations in the dystrophin gene disrupt the structure of the DGC causing severe damage to muscle fibres. In frog muscles, transmission of force laterally from an activated fibre to the muscle surface occurs without attenuation, but lateral transmission of force has not been demonstrated in mammalian muscles. A unique 'yoke' apparatus was developed that attached to the epimysium of muscles midway between the tendons and enabled the measurement of lateral force. We now report that in muscles of young wild-type (WT) mice and rats, compared over a wide range of longitudinal forces, forces transmitted laterally showed little or no decrement. In contrast, for muscles of mdx mice and very old rats, forces transmitted laterally were impaired severely. Muscles of both mdx mice and very old rats showed major reductions in the expression of dystrophin. We conclude that during contractions, forces developed by skeletal muscles of young WT mice and rats are transmitted laterally from fibre to fibre through the DGC without decrement. In contrast, in muscles of dystrophic or very old animals, disruptions in DGC structure and function impair lateral transmission of force causing instability and increased susceptibility of fibres to contraction-induced injury.

Original languageEnglish (US)
Pages (from-to)1195-1208
Number of pages14
JournalJournal of Physiology
Volume589
Issue number5
DOIs
StatePublished - Mar 2011
Externally publishedYes

ASJC Scopus subject areas

  • Physiology

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    Ramaswamy, K. S., Palmer, M. L., Van Der Meulen, J. H., Renoux, A., Kostrominova, T. Y., Michele, D. E., & Faulkner, J. A. (2011). Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats. Journal of Physiology, 589(5), 1195-1208. https://doi.org/10.1113/jphysiol.2010.201921