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Excitation-Contraction Coupling in Skeletal, Cardiac, and Smooth Muscle pp 123–136Cite as

The Functional Role of T-Tubular Calcium Channels in Skeletal Muscle Contractions

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 311))

Abstract

Nearly 35 years ago, when I began my studies on the role of calcium ions in excitation-contraction (e-c) coupling in skeletal muscle there seemed to be excellent evidence supporting the concept that the e-c coupling process was identical during twitches and depolarization contractures (Frank, 1961). For this reason in my initial studies I used high K+-induced contractures in a Na+-free solution as a model for the events occurring during e-c coupling in both types of muscle activity (Frank, 1958, 1960).

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References

  • Abdel-Latif, A.A., 1986, Calcium-mobilizing receptors, polyphosphoinositides, and the generation of second messengers. Pharmacol. Rev., 38: 227–272.

    PubMed  CAS  Google Scholar 

  • Armstrong, C.M., Bezanilla, F.M. and Horowicz, P., 1972, Twitches in the presence of ethylene glycol bis(-aminoethylether)-N, N’-tetraacetic acid, Biochim. Biophys. Acta, 267: 605–608.

    Article  PubMed  CAS  Google Scholar 

  • Beaty, G.N., Cota, G., Nicola Siri, L., Sanchez, J.A. and Stefani, E., 1987, Skeletal Muscle Ca++ channels, In Structure and Physiology of the Slow Inward Calcium Channel. 123–140, Alan R. Liss: New York.

    Google Scholar 

  • Bechem, M., Hebisc, S. and Schramm, M., 1988, Ca2+ agonists: New, sensitive probes for 2+ chanels. TIPS, 9: 257–261.

    CAS  Google Scholar 

  • Berridge, M.J., 1984, Inositol triphosphate and diacylglycerol as second messengers, Biochem. J., 220: 345–360.

    PubMed  CAS  Google Scholar 

  • Bianchi, C.P. and Shanes, A.M., 1959, Calcium influx in skeletal muscle at rest, during activity and during potassium contractures, J. Gen. Physiol., 42: 803–815.

    Article  PubMed  CAS  Google Scholar 

  • Blinks, J.R., Rüdel, R., and Taylor, S.R., 1978, Calcium transients in isolated amphibian skeletal muscle fibres: Detection with aequorin. J. Physiol. (Lond.), 277: 291–323.

    CAS  Google Scholar 

  • Bolanos, P., Caputo, C and Velar, L., 1985, Effects of Calcium, Barium and Lanthanum on Depolarization-Contraction Coupling in Skeletal Muscle Fibres of Rana Pipiens. J. Physiol. (Lond.), 370: 39–60.

    Google Scholar 

  • Brum, G., Rios, E. and Stefani, E., 1988, Effects of extracellular calcium on calcium movements of excitation-contraction coupling in frog skeletal muscle fibres. J. Physiol. (Lond.), 398: 441–473.

    CAS  Google Scholar 

  • Carrasco, M.A., Magendzo, K., Jaimovich, E. and Hidalgo, C, 1988, Calcium modulation of phosphoinositicle kinases in transverse tubule vesicles from frog skeletal muscle. Arch. Biochem. Biophys., 262: 360–366.

    Article  PubMed  CAS  Google Scholar 

  • Chadwick, C.C., Fleischer, S. and Inui, M., 1988, Identification and purification of a transverse tubule coupling protein which binds to the ryanodine receptor of terminal cisternae at the triad junction in skeletal muscle, J. Biol. Chem., 263: 10872–10877.

    PubMed  CAS  Google Scholar 

  • Curtis, B.M. and Catterall, W.A., 1986, Reconstitution of the voltage-sensitive calcium channel purified from skeletal muscle transverse tubules. Biochemistry, 11: 3077–3083.

    Article  Google Scholar 

  • Donaldson, S.K., Goldberg, N.D., Walseth, T.F. and Huetteman, D.A., 1987, Inositol trip phosphate stimulates calcium release from peeled skeletal muscle fibers. Biochim. Biophys. Acta, 927: 256–260.

    Google Scholar 

  • Fabiato, A., 1985, Rapid ionic modifications during the aequorin-detected calcium transient in a skinned canine cardiac purkinje cell, J. Gen. Physiol., 85: 189–246.

    Article  PubMed  CAS  Google Scholar 

  • Fabiato, A., 1985, Time and calcium dependence of activation and inactivation of calciuminduced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac purkinje cell. Simulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of skinned canine cardiac purkinje cell. J. Gen. Physiol., 85: 247–320.

    Article  PubMed  CAS  Google Scholar 

  • Fabiato, A., 1986, Inositol (1,4,5) triphosphate-induced versus Ca2+-induced release of Ca2+ from the cardiac sarcoplasmic reticulum. Proc. XXX Congress Int. Union of Physiol. Sciences, 16: 350.

    Google Scholar 

  • Frank, G.B., 1957, Negative after-potential of frog’s skeletal muscle. J. Neurophysiol., 20: 602–614.

    PubMed  CAS  Google Scholar 

  • Frank, G.B., 1958, Inward movement of calcium as a link between electrical and mechanical events in contraction. Nature, 182: 1800–1801.

    Article  PubMed  CAS  Google Scholar 

  • Frank, G.B., 1960, Effects of changes in extracellular calcium concentration on the potassium-induced contracture of frog’s skeletal muscle, J. Physiol., (London), 151: 518–538.

    CAS  Google Scholar 

  • Frank, G.B., 1961, Role of extracellular calcium ions in excitation-contraction coupling in skeletal muscle. In Bio-physics of physiological and pharmacological actions. American Association for the Advancement of Science, Washington, D.C., 293–307.

    Google Scholar 

  • Frank, G.B., 1962, Utilization of bound calcium in the action of caffeine and certain multivalent cations on skeletal muscle. J. Physiol. (London), 163: 254–268.

    CAS  Google Scholar 

  • Frank, G.B., 1980, Commentary: The current view of the source of trigger calcium in excitation-contraction coupling invertebrate skeletal muscle. Biochem. Pharmacol., 29: 2399–2406.

    Article  PubMed  CAS  Google Scholar 

  • Frank, G.B., 1982a, Roles of extracellular and ‘trigger’ calcium ions in excitation-contraction coupling in skeletal muscle. International Symposium on E-C Coupling, Banff, August, 1981. Can. J. Physiol. Pharmacol., 60: 427–439.

    Article  CAS  Google Scholar 

  • Frank, G.B., 1982b, The effects of reducing the extracellular calcium concentration on the twitch in isolated frog’s skeletal muscle fibres. Jap. J. Physiol., 32: 589–608.

    Article  CAS  Google Scholar 

  • Frank, G.B., 1984, Blockade of Ca++ channels inhibits K+ contractures but not twitches in skeletal muscle fibres. Can. J. Physiol. Pharmacol., 62: 374–378.

    Article  PubMed  CAS  Google Scholar 

  • Frank, G.B., 1986, A pharmacological explanation of the use-dependency of the verapamil (and D-600) block of slow calcium channels. J. Pharmacol. Exp. Ther., 236: 505–511.

    PubMed  CAS  Google Scholar 

  • Frank, G.B., 1987, Pharmacological studies of excitation-contraction coupling in skeletal muscle. Can. J. Physiol. Pharmacol., 65: 711–716.

    Article  PubMed  CAS  Google Scholar 

  • Frank, G.B., 1990, Dihydropyridine calcium channel antagonists block and agonists potentiate high potassium contractures but not twitches in frog skeletal muscle. Japanese J. Physiol., 40: 205–244.

    Article  CAS  Google Scholar 

  • Frank, G.B., Konya, L. and Sudha, T.S., 1988, Nitrendipine blocks high potassium contractures but not twitches in rat skeletal muscle. Can. J. Physiol. Pharmacol., 66: 1210–1213.

    Article  PubMed  CAS  Google Scholar 

  • Frank, G.B. and Oz, M., 1991, Use-dependent block of sodium channels by verapamil in skeletal muscle during repetitive stimulation. Proceedings of the Western Pharmacology Society, 34th Annual Meeting.

    Google Scholar 

  • Freygang, Jr., W.H., Goldstein, D.A. and Hellam, D.C., 1969, The after-potential that follows trains of impulses in frog muscle fibers. J. Gen. Physiol., 47: 929–952.

    Article  Google Scholar 

  • Fryer, M.W., Neering, I.R., 1986, Relationship between intracellular calcium concentration and relaxation of fastnd slow muscles. Neurosci. Lett., 64: 231–235.

    Article  PubMed  CAS  Google Scholar 

  • Gage, P.W. and Eisenberg, R.S., 1969, Action potentials, after-potentials and excitation-contraction coupling in frog sartorius muscle fibres without transverse tubules. J. Gen. Physiol., 53: 298–310.

    Article  PubMed  CAS  Google Scholar 

  • Gallant, E.M. and Goettl, V.M., 1985, Effects of calcium antagonists on mechanical responses of mammalian skeletal muscles. Eur. J. Pharmacol., 117: 259–265.

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Serratos, H., Valley-Aguilera, R., Lathrop, D.A., del Carmen Garcia, M., 1982, Slow inward calcium currents have no obvious role in muscle excitation-contraction coupling. Nature 298: 292–294.

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo, C., Carrasco, M.A., Magendzo, K. and Jaimovich, E., 1986, Phosphorylation of phosphatidylinositol by transverse tubule vesicles and its possible role in excitation-contraction coupling. FEBS Lett., 202: 69–73.

    Article  PubMed  CAS  Google Scholar 

  • Horiuti, K., 1988, Mechanism of contracture on cooling of caffeine-treated frog skeletal muscle fibres. J. Physiol. (Lond.), 398: 131–148.

    CAS  Google Scholar 

  • Hui, C.S., Eisenberg, R.S. and Milton, R.L., 1984, Charge movement in skeletal muscle fibers paralysed by the calcium-entry blocker D600. Proc. Natl. Acad. Sci. U.S.A., 81: 2582–2585.

    Article  PubMed  CAS  Google Scholar 

  • Hui, C.S. and Milton, R., 1987, Suppression of charge movement in frog skeletal muscle by D600. J. Muscle Res. Cell Motil., 3: 195–208.

    Article  Google Scholar 

  • Ildefonse, M., Fosset, M., Lazdunski, M., Renaud, J.F. and Rougier, O., 1985, Excitation contraction coupling in skeletal muscle: Evidence for a role of slow Ca2+ channel activators and inhibitors in the dihydropyridine series. Biochem. Biophvs. Res. Commun., 129: 904–909.

    Article  CAS  Google Scholar 

  • Lamb, G.D., 1986, Components of charge movement in rabbit skeletal muscle: The effect of tetracaine and nifedipine. J. Physiol. (Lond.), 376: 85–100.

    CAS  Google Scholar 

  • Lamb, G.D. and Walsh, T., 1987, Calcium currents, charge movement and dihydropyridine binding in fast- and slow-twitch muscles of rat and rabbit. J. Physiol. (Lond.), 393: 595–617.

    CAS  Google Scholar 

  • Kernell, D., 1965, High-frequency repetitive firing of cat lumbosacral motorneurones stimulated by long-lasting injected currents. Acta Physiol. Scand., 65: 74–86.

    Article  Google Scholar 

  • Kirsch, G.E., Nichols, R.A. and Nakajima, S., 1977, Delayed rectification in the transverse tubules. J. Gen. Physiol. 70: 1–21.

    Article  PubMed  CAS  Google Scholar 

  • Kotsias, B.A. and Muchnik, S., 1985, Frequency-dependent effect of verapamil on rat soleus muscle. Experientia, 41:1538–1540.

    Article  PubMed  CAS  Google Scholar 

  • Lea, T.J., Griffiths, P.J., Tregear, R.T. and Ashley, C.C., 1986, An examination of the ability of inositol 1,4,5-triphosphate to induce calcium release and tension development in skinned skeletal muscle fibres of frog and crustacea. FEBS Lett., 207: 153–161.

    Article  PubMed  CAS  Google Scholar 

  • Lee, K.S. and Tsien, R.W., 1983, Mechanism of calcium channel blockade by verapamil, D600, diltiazem and nitrendipine in single dialysed heart cells. Nature (Lond.), 302: 790–794.

    Article  CAS  Google Scholar 

  • Lopez, E., 1982 Post-tetanic potentiation and inhibition in single fibres isolated from frog semitendinosus muscle. Jpn. J. Physiol., 32: 103–119.

    Article  PubMed  CAS  Google Scholar 

  • Mikos, G.J. and Snow, T.R., 1987, Failure of inositol 1,4,5-trisphosphate to elicit or potentiate Ca++ release from isolated skeletal muscle sarcoplasmic reticulum. Biochim. Biophys. Acta, 927: 256–260.

    Article  PubMed  CAS  Google Scholar 

  • Nosek, T.M., Williams, M.F., Zeigler, S.T. and Godt, R.E., 1986, Inositol triphosphate enhances calcium release in skinned cardiac and skeletal muscle. Am. J. Physiol., 250: C807–811.

    PubMed  CAS  Google Scholar 

  • Ogawa, Y. and Tanokura, M., 1986b, Kinetic studies of calcium binding to parvalbumin from bullfrog skeletal muscle. J. Biochem. (Tokyo), 99: 81–89.

    CAS  Google Scholar 

  • Oz, M. and Frank, G.B., 1991, Decrease in the size of tetanic responses produced by nitrendipine or by extracellular Ca++ ion removal without blocking twitches or action potentials in skeleal muscle. J. Pharmacol. Exp. Ther., 257, No. 2., 575–581.

    PubMed  CAS  Google Scholar 

  • Rios, E. and Brum, G., 1987, Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature, 325: 717–720.

    Article  PubMed  CAS  Google Scholar 

  • Rios, E. and Pizarro, G., 1988, Voltage sensors and calcium channels of excitation-contraction coupling. N.I.P.S., 3: 223–227.

    Google Scholar 

  • Schneider, M.F. and Chandler, W.K., 1973, Voltage dependent charge movement in skeletal muscle: A possible step in excitation-contraction coupling. Nature, 242: 244.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz, L.M., McCleskey, W. and Almers, W., 1985, Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. Nature, 314: 747–751.

    Article  PubMed  CAS  Google Scholar 

  • Snyder, S.H. and Pert, C.B., 1975, Opiate receptor mechanisms. Neurosci. Res. Prog. Bull., 13: 26–34.

    CAS  Google Scholar 

  • Solandt, D.Y., 1936, The effect of potassium on the excitability and resting metabolism of frog’s muscle. J. Physiol. (Lond.), 86: 162–170.

    CAS  Google Scholar 

  • Somlyo, A.V., McClellan, G., Gonzalez-Serratos, H., Somlyo, A.P., 1985, Electron probe X-ray microanalysis of post-tetanic Ca2+ and Mg2+ movements across the sarcoplasmic reticulum in situ. J. Biol. Chem., 260: 6801–6807.

    PubMed  CAS  Google Scholar 

  • Suda, N. and Kurihara, S., 1991, Intracellular calcium signals measured with Fura-2 and Aequorin in frog skeletal muscle fibers. Jpn. J. Physiol., 41: 277–295.

    Article  PubMed  CAS  Google Scholar 

  • Thieleczek, R. and Heilmeyer, Jr., L.M.G., 1986, Inositol 1,4,5-triphosphate enhances Ca2+-sensitivity of the contractile mechanism of chemically skinned rabbit skeletal muscle fibers. Biochem. Biophys. Res. Commun., 135: No. 2, 662–669.

    Article  PubMed  CAS  Google Scholar 

  • Vergara, J. and Delay, M., 1986, A transmission delay and the effect of temperature at the triadic junction of skeletal muscle. Proc. R. Soc. Lond. (Biol.), 229: 97–110.

    Article  CAS  Google Scholar 

  • Vergara, J., Tsien, R.Y. and Delay, M., 1985, Inositol 1,4,5-triphosphate: a possible chemical link in excitation-contraction coupling in muscle. Proc. Natl. Acad. Sci. USA, 82: 6352–6356.

    Article  PubMed  CAS  Google Scholar 

  • Volpe, P., Di Virgilio, F., Pozzan, T. and Salviati, G., 1986, Role of inositol 1,4,5-triphosphate in excitation-contraction coupling in skeletal muscle. FEBS Lett., 197: 1–4.

    Article  PubMed  CAS  Google Scholar 

  • Volpe, P., Salviati, G., Di Virgilio, F. and Pozzan, T., 1985, Inositol 1,4,5-triphosphate induces calcium release from sarcoplasmic reticulum of skeletal muscle. Nature, 316: 347–349.

    Article  PubMed  CAS  Google Scholar 

  • Vos, E.C. and Frank, G.B., 1972a, The threshold for potassium-induced contractures of frog skeletal muscle. Potentiation of potassium-induced contractures by pre-exposure to subthreshold potassium concentrations. Can. J. Physiol. Pharmacol., 50: 37–44.

    Article  CAS  Google Scholar 

  • Vos, E.C. and Frank, G.B., 1972b, Events occurring in the region of the threshold for potassium-induced contractures of frog skeletal muscle. Changes in elasticity and oxygen consumption. Can. J. Physiol. Pharmacol., 50: 179–187.

    Article  CAS  Google Scholar 

  • Walker, J.W., Somlyo, A.V., Goldman, Y.E., Somylo, A.P. and Trentham, D.R., 1987, Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-triphosphate. Nature, 327: 249–252.

    Article  PubMed  CAS  Google Scholar 

  • Walsh, K.P., Bryant, S.H. and Schwartz, A., 1987, Suppression of charge movement by calcium antagonists is not related to calcium channel block. Pflugers Arch., 409: 217–219.

    Article  PubMed  CAS  Google Scholar 

  • Weiss, G.B. and Bianchi, C.P., 1965, The effect of potassium concentration on Ca45 uptake in frog sartorius muscle. J. Cell. Comp. Physiol., 65: 385–392.

    Article  CAS  Google Scholar 

  • Zhu, P.H., Miledi, R. and Parker, I., 1986, Minimal latency of calcium release in frog twitch muscle fibres. Proc. R. Soc. Lond. (Biol.), 229: 39–46.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, University of Alberta, 9-70 Medical Sciences Building, Edmonton, Alberta, Canada, T6C 2H7

    George B. Frank & Murat Öz

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  1. George B. Frank
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  2. Murat Öz
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Editors and Affiliations

  1. University of Alberta, Edmonton, Alberta, Canada

    George B. Frank

  2. Thomas Jefferson University, Philadelphia, Pennsylvania, USA

    C. Paul Bianchi

  3. University of Calgary, Calgary, Alberta, Canada

    Henk E. D. J. ter Keurs

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Frank, G.B., Öz, M. (1992). The Functional Role of T-Tubular Calcium Channels in Skeletal Muscle Contractions. In: Frank, G.B., Bianchi, C.P., ter Keurs, H.E.D.J. (eds) Excitation-Contraction Coupling in Skeletal, Cardiac, and Smooth Muscle. Advances in Experimental Medicine and Biology, vol 311. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3362-7_9

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