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Altered Ca2+-handling in human skeletal muscle to alleviate Ca2+-induced damage in the days associated with delayed onset muscle soreness

T.R. Cully,1 R.M. Murphy,2 L. Roberts,3,4 T. Raastad,5 R.G. Fassett,3 J.S. Coombes,3 I.D. Jayasinghe1,6 and B.S. Launikonis,1 1School of Biomedical Sciences, The University of Queensland, Brisbane, QLD 4072, Australia, 2Department of Biochemistry & Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, VIC 3084, Australia, 3School of Human Movement and Nutritional Sciences, The University of Queensland, Brisbane, QLD 4072, Australia, 4Centre of Excellence for Applied Sport Science Research, Queensland Academy of Sport, Brisbane, QLD 4111, Australia, 5Norwegian School of Sport Sciences, Oslo N-0806, Norway and 6School of Biomedical Sciences, University of Leeds, Leeds LS2 9JT, UK.

High-force eccentric exercise results in sustained increases in the Ca2+ levels in the cytoplasm ([Ca2+]cyto), which potentially may cause damage to the muscle. The muscle has been observed to form vacuoles which remained in contact with the plasmalemma post-eccentric contraction, in mouse studies (Yeung et al., 2002). The plasmalemma of skeletal muscle mostly consists of tubules that are invaginations of the outer membrane. This membrane network inside the fibres is commonly referred to as the tubular (t-) system. Three-dimensional reconstruction of the human muscle fibre t-system showed regular, transverse tubules and series of longitudinal tubules that often join transverse tubules across misregistered sarcomeres. Longitudinal tubules were prevalent at the periphery of the fibre. A heavy-load strength training bout caused the loss of the predominantly transverse organisation of the t-system and an increase in the propensity of the longitudinal tubules to form a series of large vacuoles across adjacent sarcomeres. Acute application of high [Ca2+]cyto could also induce vacuolation. The transverse tubules and vacuoles displayed distinct Ca2+-handling properties. Both components of the t-system could take up Ca2+ from the cytoplasm but only transverse tubules supported store-operated Ca2+ entry (SOCE) during Ca2+ release. The retention of significant volumes of Ca2+ within vacuoles during SOCE provides an effective buffer of [Ca2+]cyto to reduce the total content of Ca2+ within the fibre. These results indicate that the human muscle t-system can alter its structure to change its Ca2+ handling properties. We propose this ability can reduce or limit resistance exercise-induced, Ca2+-dependent damage to the fibre by the reduction of [Ca2+]cyto to help maintain fibre viability during the period associated with delayed onset muscle soreness.

Yeung EW, Balnave CD, Ballard HJ, Bourreau J-P & Allen DG (2002). Development of T-tubular vacuoles in eccentrically damaged mouse muscle fibres. J Physiol 540, 581-592.