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Calcium signaling in isolated skeletal muscle fibers investigated under “silicone voltage-clamp” conditions

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Abstract

In skeletal muscle, release of calcium from the sarcoplasmic reticulum (SR) represents the major source of cytoplasmic Ca2+ elevation. SR calcium release is under the strict command of the membrane potential, which drives the interaction between the voltage sensors in the t-tubule membrane and the calcium-release channels. Either detection or control of the membrane voltage is thus essential when studying intracellular calcium signaling in an intact muscle fiber preparation. The silicone-clamp technique used in combination with intracellular calcium measurements represents an efficient tool for such studies. This article reviews some properties of the plasma membrane and intracellular signals measured with this methodology in mouse skeletal muscle fibers. Focus is given to the potency of this approach to investigate both fundamental aspects of excitation-contraction coupling and potential alterations of intracellular calcium handling in some muscle diseases.

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References

  1. Melzer, W., Herrmann-Frank, A., and Luttgau, H. C. (1995) The role of Ca2+ ions in excitationcontraction coupling of skeletal muscle fibres. Biochim. Biophys. Acta 1241, 59–116.

    PubMed  Google Scholar 

  2. Franzini-Armstrong, C. and Protasi, F. (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol. Rev. 77, 699–729.

    PubMed  CAS  Google Scholar 

  3. Dulhunty, A. F., Haarmann, C. S., Green, D., Laver, D. R., Board, P. G., and Casarotto M. G. (2002) Interactions between dihydropyridine receptors and ryanodine receptors in striated muscle. Prog. Biophys. Mol. Biol. 79, 45–75.

    Article  PubMed  CAS  Google Scholar 

  4. Meissner, G. (1994) Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56, 485–508.

    Article  PubMed  CAS  Google Scholar 

  5. Xu, L., Tripathy, A., Pasek, D. A., and Meissner, G. (1998) Potential for pharmacology of ryanodine receptor/calcium release channels. Annu. NY Acad. Sci. 853, 130–148.

    Article  CAS  Google Scholar 

  6. Rios, E., Pizarro, G., and Stefani, E. (1992) Charge movement and the nature of signal transduction in skeletal muscle excitation-contraction coupling. Annu. Rev. Physiol. 54, 109–133.

    Article  PubMed  CAS  Google Scholar 

  7. Schneider, M. F. (1994). Control of calcium release in functioning skeletal muscle fibers. Annu. Rev. Physiol. 56, 463–484.

    Article  PubMed  CAS  Google Scholar 

  8. Jacquemond, V. (1997) Indo-1 fluorescence signals elicited by membrane depolarization in enzymatically isolated mouse skeletal muscle fibers. Biophys. J. 73, 920–928.

    PubMed  CAS  Google Scholar 

  9. Collet, C., Allard, B., Tourneur, Y., and Jacquemond, V. (1999) Intracellular calcium signals measured with indo-1 in isolated skeletal muscle fibres from control and mdx mice. J. Physiol. (Lond.) 520, 417–29.

    Article  CAS  Google Scholar 

  10. Collet, C. and Jacquemond, V. (2002) Sustained release of calcium elicited by membrane depolarization in ryanodine-injected mouse skeletal muscle fibers. Biophys. J. 82, 1509–1523.

    PubMed  CAS  Google Scholar 

  11. Jacquemond, V. and Allard, B. (1998) Activation of Ca2+-activated K+ channels by an increase in intracellular Ca2+ induced by depolarization of mouse skeletal muscle fibres. J. Physiol. (Lond.) 509, 93–102.

    Article  CAS  Google Scholar 

  12. Collet, C., Strube, C., Csernoch, L., Mallouk, N., Ojeda, C., Allard, B., et al. (2002) Effects of extracellular ATP on freshly isolated mouse skeletal muscle cells during pre-natal and post-natal development. Pflugers Arch. 443, 771–778.

    Article  PubMed  CAS  Google Scholar 

  13. Collet, C., Csernoch, L., and Jacquemond, V. (2003) Intramembrane charge movement and L-type calcium current in skeletal muscle fibers isolated from control and mdx mice. Biophys. J. 84, 251–265.

    Article  PubMed  CAS  Google Scholar 

  14. Rios, E. and Pizarro, G. (1991) Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol. Rev. 71, 849–908.

    PubMed  CAS  Google Scholar 

  15. Delbono, O. (1992) Calcium current activation and charge movement in denervated mammalian skeletal muscle fibres. J. Physiol. (Lond) 451, 187–203.

    CAS  Google Scholar 

  16. Szentesi, P., Jacquemond, V., Kovacs, L., and Csernoch, L. (1997) Intramembrane charge movement and sarcoplasmic calcium release in enzymatically isolated mammalian skeletal muscle fibres. J. Physiol. (Lond.) 505, 371–384.

    Article  CAS  Google Scholar 

  17. Donaldson, P. L., and Beam, K. G. (1983) Calcium currents in a fast-twitch skeletal muscle of the rat. J. Gen. Physiol. 82, 449–468.

    Article  PubMed  CAS  Google Scholar 

  18. Szentesi, P., Collet, C., Sarkozi, S., Szegedi, C., Jona, I., Jacquemond, V., et al. (2001) Effects of dantrolene on steps of excitation-contraction coupling in mammalian skeletal muscle fibers. J. Gen. Physiol. 118, 355–375.

    Article  PubMed  CAS  Google Scholar 

  19. Friedrich, O., Ehmer, T., and Fink, R. H. (1999) Calcium currents during contraction and shortening in enzymatically isolated murine skeletal muscle fibres. J. Physiol. (Lond.) 15, 757–770.

    Article  Google Scholar 

  20. Gyorke, S. and Palade, P. (1992) Effects of perchlorate on excitation-contraction coupling in frog and crayfish skeletal muscle. J. Physiol. (Lond.) 456, 443–451.

    CAS  Google Scholar 

  21. Klein, M. G., Simon, B. J., Szucs, G., and Schneider, M. F. (1988) Simultaneous recording of calcium transients in skeletal muscle using high- and low-affinity calcium indicators. Biophys. J. 53, 971–988.

    PubMed  CAS  Google Scholar 

  22. Baylor, S. M. and Hollingworth, S. (2000) Measurement and interpretation of cytoplasmic [Ca2+] signals from calcium-indicator dyes. News Physiol. Sci., 15, 19–26.

    PubMed  CAS  Google Scholar 

  23. Delbono, O., and Stefani, E. (1993) Calcium transients in single mammalian skeletal muscle fibres. J. Physiol. (Lond.) 463, 689–707.

    CAS  Google Scholar 

  24. Garcia, J. and Schneider, M. F., (1993) Calcium transients and calcium release in rat fast-twitch skeletal muscle fibres. J. Physiol. (Lond.) 463, 709–728.

    CAS  Google Scholar 

  25. Baylor, S. M., Chandler, W. K., and Marshall, M. W. (1983) Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J. Physiol. (Lond.), 344, 625–666.

    CAS  Google Scholar 

  26. Maylie, J., Irving, M., Sizto, N. L., and Chandler, W. K. (1987) Calcium signals recorded from cut frog twitch fibers containing antipyrylazo III. J. Gen. Physiol. 89, 83–143.

    Article  PubMed  CAS  Google Scholar 

  27. Csernoch, L., Bernengo, J. C., Szentesi, P., and Jacquemond, V. (1998) Measurements of intracellular Mg2+ concentration in mouse skeletal muscle fibers with the fluorescent indicator mag-indo-1. Biophys. J. 75, 957–967.

    PubMed  CAS  Google Scholar 

  28. Baylor, S. M. and Hollingworth, S. (1988) Fura-2 calcium transients in frog skeletal muscle fibres. J. Physiol. (Lond.) 403, 151–192.

    CAS  Google Scholar 

  29. Lattanzio, F. A. and Bartschat, D. K. (1991) The effect of pH on rate constants, ion selectivity and thermodynamic properties of fluorescent calcium and magnesium indicators. Biochem. Biophys. Res. Commun., 177, 184–191.

    Article  PubMed  CAS  Google Scholar 

  30. Gillis, J. M. (1999) Understanding dystrophinopathies: an inventory of the structural and functional consequences of the absence of dystrophin in muscles of the mdx mouse. J. Muscle Res. Cell. Motil. 20, 605–625.

    Article  PubMed  CAS  Google Scholar 

  31. Blake, D. J., Weir, A., Newey, S. E., and Davies, K. E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82, 291–329.

    PubMed  CAS  Google Scholar 

  32. Tutdibi, O., Brinkmeier, H., Rudel, R., and Fohr, K. J. (1999) Increased calcium entry into dystrophin-deficient muscle fibres of MDX and ADR-MDX mice is reduced by ion channel blockers. J. Physiol. (Lond.) 515, 859–868.

    Article  CAS  Google Scholar 

  33. Mallouk, N., Jacquemond, V., and Allard, B. (2000) Elevated subsarcolemmal Ca2+ in mdx mouse skeletal muscle fibers detected with Ca2+-activated K+ channels. Proc. Natl. Acad. Sci. USA 97, 4950–4955.

    Article  PubMed  CAS  Google Scholar 

  34. Mallouk, N. and Allard, B. (2002) Ca2+ influx and opening of Ca2+-activated K+ channels in muscle fibers from control and mdx mice. Biophys. J. 82, 3012–3021.

    PubMed  CAS  Google Scholar 

  35. Kargacin, M. E. and Kargacin, G. J. (1996) The sarcoplasmic reticulum calcium pump is functionally altered in dystrophic muscle. Biochim. Biophys. Acta, 1290, 4–8.

    PubMed  Google Scholar 

  36. Divet, A., and Huchet-Cadiou, C. (2002) Sarcoplasmic reticulum function in slow- and fast-twitch skeletal muscles from mdx mice. Pflugers Arch. 444, 634–643.

    Article  PubMed  CAS  Google Scholar 

  37. Robert, V., Massimino, M. L., Tosello, V., Marsault, R., Cantini, M., Sorrentino, V., et al. (2001) Alteration in calcium handling at the subcellular level in mdx myotubes. J. Biol. Chem. 276, 4647–4651.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Physiologie des Eléments Excitables, Université Claude Bernard Lyon 1, UMR CNRS 5123, F69622, Villeurbanne, France

    Claude Collet, Sandrine Pouvreau, Bruno Allard & Vincent Jacquemond

  2. Department of Physiology; Health Sciences Centre, University of Debrecen, H-4012, Debrecen, Hungary

    Laszlo Csernoch

Authors
  1. Claude Collet
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  2. Sandrine Pouvreau
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  3. Laszlo Csernoch
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  4. Bruno Allard
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  5. Vincent Jacquemond
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Correspondence to Vincent Jacquemond.

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Collet, C., Pouvreau, S., Csernoch, L. et al. Calcium signaling in isolated skeletal muscle fibers investigated under “silicone voltage-clamp” conditions. Cell Biochem Biophys 40, 225–236 (2004). https://doi.org/10.1385/CBB:40:2:225

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