Mechanisms of excitation-contraction uncoupling relevant to activity-induced muscle fatigue

Applied Physiology, Nutrition and Metabolism

Volumn 34, Issue 3, 2009, Pages 368-372

  Lamb, Graham D ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

Calpain; eccentric contraction; Excitation contraction coupling; Muscle fatigue; Muscle weakness; Muscular dystrophy; Ryanodine receptor; Sarcoplasmic reticulum; Skeletal muscle; Skinned fiber

Indexed keywords

CALCIUM;

EXERCISE; HUMAN; METABOLISM; MUSCLE CONTRACTION; MUSCLE FATIGUE; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE;

CALCIUM; EXERCISE; HUMANS; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL;

EID: 67651231034     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H09-032     Document Type: Review

References (40)

1. Allen, D.G., Whitehead, N.P., and Yeung, E.W. 2005. Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes. J. Physiol. 567: 723-735. doi:10.1113/jphysiol.2005.091694. PMID:16002444.
2. Allen, D.G., Lamb, G.D., and Westerblad, H. 2008. Skeletal muscle fatigue: cellular mechanisms. Physiol. Rev. 88: 287-332. doi:10.1152/physrev.00015.2007. PMID:18195089.
3. Bakker, A.J., Lamb, G.D., and Stephenson, D.G. 1996. The effect of 2,5-di-(tert-butyl)-1,4-hydroquinone on force responses and the contractile apparatus in mechanically skinned muscle fibres of the rat and toad. J. Muscle Res. Cell Motil. 17: 55-67. doi:10.1007/BF00140324. PMID:8740432.
4. Balnave, C.D., and Allen, D.G. 1995. Intracellular calcium and force in single mouse muscle fibres following repeated contractions with stretch. J. Physiol. 488: 25-36. PMID:8568662.
5. Baylor, S.M., and Hollingworth, S. 2003. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J. Physiol. 551: 125-138. doi:10.1113/jphysiol.2003.041608. PMID:12813151.
6. Bellinger, A.M., Reiken, S., Dura, M., Murphy, P.W., Deng, S.X., Landry, D.W., et al. 2008. Remodeling of ryanodine receptor complex causes "leaky" channels: a molecular mechanism for decreased exercise capacity. Proc. Natl. Acad. Sci. U.S.A. 105: 2198-2202. doi:10.1073/pnas.0711074105. PMID:18268335.
7. Bellinger, A.M., Reiken, S., Carlson, C., Mongillo, M., Liu, X., Rothman, L., et al. 2009. Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med., In press. PMID:19198614.
8. Bruton, J.D., Place, N., Yamada, T., Silva, J.P., Andrade, F.H., Dahlstedt, A.J., et al. 2008. Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J. Physiol. 586: 175-184. doi:10.1113/jphysiol.2007.147470. PMID:18006575.
9. 2+] in the development of low frequency fatigue in mouse single muscle fibres. J. Physiol. 491: 813-824. PMID: 8815213.
10. Chin, E.R., Balnave, C.D., and Allen, D.G. 1997. Role of intracellular calcium and metabolites in low-frequency fatigue of mouse skeletal muscle. Am. J. Physiol. 272: C550-C559. PMID: 9124298.
11. Duguez, S., Bartoli, M., and Richard, I. 2006. Calpain 3: a key regulator of the sarcomere? FEBS J. 273: 3427-3436. doi:10.1111/j.1742-4658.2006.05351.x. PMID:16884488.
12. Dulhunty, A.F. 2006. Excitation-contraction coupling from the 1950s into the new millennium. Clin. Exp. Pharmacol. Physiol. 33: 763-772. doi:10.1111/j.1440-1681.2006.04441.x. PMID: 16922804.
13. Durham, W.J., Aracena-Parks, P., Long, C., Rossi, A.E., Goonasekera, S.A., Boncompagni, S., et al. 2008. RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice. Cell, 133: 53-65. doi:10.1016/j.cell.2008.02.042. PMID:18394989.
14. Dutka, T.L., and Lamb, G.D. 2004. Effect of low cytoplasmic [ATP] on excitation-contraction coupling in fast-twitch muscle fibres of the rat. J. Physiol. 560: 451-468. doi:10.1113/jphysiol.2004.069112. PMID:15308682.
15. Gilchrist, J.S., Wang, K.K., Katz, S., and Belcastro, A.N. 1992. Calcium-activated neutral protease effects upon skeletal muscle sarcoplasmic reticulum protein structure and calcium release. J. Biol. Chem. 267: 20857-20865. PMID:1400400.
16. Goll, D.E., Thompson, V.F., Li, H., Wei, W., and Cong, J. 2003. The calpain system. Physiol. Rev. 83: 731-801. PMID: 12843408.
17. Ingalls, C.P., Warren, G.L., Williams, J.H., Ward, C.W., and Armstrong, R.B. 1998. E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J. Appl. Physiol. 85: 58- 67. PMID:9655756.
18. Inomata, M., Nomoto, M., Hayashi, M., Nakamura, M., Imahori, K., and Kawashima, S. 1984. Comparison of low and high calcium requiring forms of the calcium-activated neutral protease (CANP) from rabbit skeletal muscle. J. Biochem. 95: 1661- 1670. PMID:6088474.
19. Kim, K.C., Caswell, A.H., Brunschwig, J.P., and Brandt, N.R. 1990. Identification of a new subpopulation of triad junctions isolated from skeletal muscle; morphological correlations with intact muscle. J. Membr. Biol. 113: 221-235. doi:10.1007/BF01870074. PMID:2159516.
20. Kramerova, I., Kudryashova, E., Tidball, J.G., and Spencer, M.J. 2004. Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum. Mol. Genet. 13: 1373-1388. doi:10.1093/hmg/ddh153. PMID:15138196.
21. Lamb, G.D. 2002. Excitation-contraction coupling and fatigue mechanisms in skeletal muscle: studies with mechanically skinned fibres. J. Muscle Res. Cell Motil. 23: 81-91. doi:10.1023/A:1019932730457. PMID:12363289.
22. 2+] on excitation-contraction coupling in skeletal muscle fibres of the rat. J. Physiol. 478: 331-339. PMID: 7965848.
23. 2+] abolishes excitation-contraction coupling in skeletal muscle fibres of rat and toad. J. Physiol. 489: 349-362. PMID:8847631.
24. 2+ entry and the inositol trisphosphate receptor. Proc. Natl. Acad. Sci. U.S.A. 100: 2941-2944. doi:10.1073/pnas.0536227100. PMID:12601149.
25. 2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim. Biophys. Acta, 1241: 59-116. PMID: 7742348.
26. 2+] and is not dependent on stretch. J. Biol. Chem., In press. PMID:19144634.
27. Murphy, R.M., Snow, R.J., and Lamb, G.D. 2006a. mu-Calpain and calpain-3 are not autolyzed with exhaustive exercise in humans. Am. J. Physiol. Cell Physiol. 290: C116-C122. doi:10.1152/ajpcell.00291.2005. PMID:16107503.
28. 2+-activation of diffusible and bound pools of {micro}-calpain in rat skeletal muscle. J. Physiol. 576: 595-612. doi:10.1113/jphysiol.2006.114090. PMID:16857710.
29. Murphy, R.M., Goodman, C.A., McKenna, M.J., Bennie, J., Leikis, M., and Lamb, G.D. 2007. Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise. J. Appl. Physiol. 103: 926-931. doi:10.1152/japplphysiol.01422.2006. PMID:17585039.
30. Ono, Y., Kakinuma, K., Torii, F., Irie, A., Nakagawa, K., Labeit, S., et al. 2004. Possible regulation of the conventional calpain system by skeletal muscle-specific calpain, p94/calpain 3. J. Biol. Chem. 279: 2761-2771. doi:10.1074/jbc.M308789200. PMID:14594950.
31. Pedersen, T.H., Nielsen, O.B., Lamb, G.D., and Stephenson, D.G. 2004. Intracellular acidosis enhances the excitability of working muscle. Science, 305: 1144-1147. doi:10.1126/science.1101141. PMID:15326352.
32. Posterino, G.S., Lamb, G.D., and Stephenson, D.G. 2000. Twitch and tetanic force responses and longitudinal propagation of action potentials in skinned skeletal muscle fibres of the rat. J. Physiol. 527: 131-137. doi:10.1111/j.1469-7793.2000.t01-200131.x. PMID:10944176.
33. Raynaud, F., Bonnal, C., Fernandez, E., Bremaud, L., Cerutti, M., Lebart, M.C., et al. 2003. The calpain 1-alpha-actinin interaction. Resting complex between the calcium-dependent protease and its target in cytoskeleton. Eur. J. Biochem. 270: 4662-4670. doi:10.1046/j.1432-1033.2003.03859.x. PMID:14622253.
34. Raynaud, F., Fernandez, E., Coulis, G., Aubry, L., Vignon, X., Bleimling, N., et al. 2005. Calpain 1-titin interactions concentrate calpain 1 in the Z-band edges and in the N2-line region within the skeletal myofibril. FEBS J. 272: 2578-2590. doi:10.1111/j.1742-4658.2005.04683.x. PMID:15885106.
35. Sorimachi, H., Toyama-Sorimachi, N., Saido, T.C., Kawasaki, H., Sugita, H., Miyasaka, M., et al. 1993. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268: 10593-10605. PMID:8486713.
36. Stephenson, D.G., Lamb, G.D., and Stephenson, G.M. 1998. Events of the excitation-contraction-relaxation (E-C-R) cycle in fast-and slow-twitch mammalian muscle fibres relevant to muscle fatigue. Acta Physiol. Scand. 162: 229-245. doi:10.1046/j.1365-201X.1998.0304f.x. PMID:9578368.
37. 2+-activated proteases in toad muscle fibres. J. Physiol. 564: 775-790. doi:10.1113/jphysiol.2004.082180. PMID:15746171.
38. 2+ concentration during contractions. Am. J. Physiol. Cell Physiol. 290: C1199-C1208. doi:10.1152/ajpcell.00469.2005. PMID:16306125.
39. 2+-induced disruption of excitation-contraction coupling in mammalian skeletal muscle fibers.. Am. J. Physiol. Cell Physiol. [Epub ahead of print.] doi:10.1152/ajpcell.00008.2009. PMID:19295178.
40. Whitehead, N.P., Yeung, E.W., and Allen, D.G. 2006. Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin. Exp. Pharmacol. Physiol. 33: 657-662. doi:10.1111/j.1440-1681.2006.04394.x. PMID:16789936.