Summary
The segmented trunk muscle (myotome muscle) of the lancelet (Branchiostoma lanceolatum), a pre-vertebrate chordate, was studied in order to gain information regarding the evolution of excitation-contraction (EC) coupling.
Myotome membrane vesicles could be separated on isopycnic sucrose gradients into two main fractions, probably comprising solitary microsomes and diads of plasma membrane and sarcoplasmic reticulum, respectively. Both fractions bound the dihydropyridine PN 200/110 and the phenylalkylamine (−)D888 (devapamil) while specific ryanodine binding was observed in the diad preparation only. Pharmacological effects on Ca2+ currents measured under voltage-clamp conditions in single myotome fibers included a weak block by the dihydropyridine nifedipine and a shift of the voltage dependences of inactivation and restoration to more negative potentials by (−)D888. After blocking the Ca2+ current by cadmium in voltage-clamped single fibers, the contractile response persisted and a rapid intramembrane charge movement could be demonstrated. Both responses exhibited a voltage sensitivity very similar to the one of the voltage-activated Ca2+ channels.
Our biochemical and electrophysiological results indicate that the EC coupling mechanism of the protochordate myotome cell is similar to that of the vertebrate skeletal muscle fiber: Intracellular Ca2+ release, presumably taking place via the ryanodine receptor complex, is under control of the cell membrane potential. The sarcolemmal Ca2+ channels might serve as voltage sensors for this process.
Similar content being viewed by others
References
Ashley, C.C., Mulligan, I.P., Lea, T.J. 1991. Ca2+ and activation mechanisms in skeletal muscle. Q. Rev. Biophys. 24:1–73
Bean, B.P. 1984. Nitrendipine block of cardiac calcium channels: High-affinity binding to the inactivated state. Proc. Natl. Acad. Sci. USA 81:6388–6392
Benterbusch, R., Melzer, W. 1992. Ca2+ current in myotome cells of the lancelet (Branchiostoma lanceolatum). J. Physiol. 450:437–453
Berwe, D., Gottschalk, G., Lüttgau, H.C. 1987. Effects of the calcium antagonist gallopamil (D600) upon excitation-contraction coupling in toe muscle fibres of the frog. J. Physiol. 385:693–707
Block, B.A., Imagawa, T., Campbell, K.P., Franzini-Armstrong, C. 1988. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 107:2587–2600
Bortz, J. 1979. Lehrbuch der Statistik. Springer-Verlag, Berlin
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254
Brandt, N.R. 1985. Identification of two populations of cardiac microsomes with nitrendipine receptors: Correlation of the distribution of dihydropyridine receptors with organelle specific markers. Arch. Biochem. Biophys. 242:306–319
Brum, G., Rios, E., Stefani, E. 1988. Effects of extracellular calcium on calcium movements of excitation-contraction coupling in frog skeletal muscle fibres. J. Physiol. 398:441–473
Campbell, K.P., MacLennan, D.H., Jorgensen, A.O. 1983. Staining of Ca2+ binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye “Stainsall.” J. Biol. Chem. 258:11267–11273
Caswell, A.H., Lau, Y.H., Brunschwig, J.-P. 1976. Ouabain-binding vesicles from skeletal muscle. Arch. Biochem. Biophys. 176:417–430
Dorit, R.L., Walker, W.F., Barnes, R.D. 1991. Zoology, pp. 804–813. Sounders College Publishing, Philadelphia
Dumont, L., Williams, J.S., Vaghy, P.L., Schwartz, A. 1988. Characteristics of the phenylalkylamine binding site in canine cardiac sarcolemmal membranes. Basic Res. Cardiol. 83:369–375
Dux, L., Lelkes, G., Hieu, L.H., Nemcsok, J. 1989. Structural differences between the Ca2+-ATPase enzymes of sarcoplasmic reticulum membrane from rabbit and carp muscles. Comp. Biochem. Physiol. 92B:263–270
Erdmann, R., Lüttgau, H.C. 1989. The effect of the phenylalkylamine D888 (devapamil) on force and Ca2+ current in isolated frog skeletal muscle fibres. J. Physiol. 413:521–541
Fabiato, A. 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 245:C1-C14
Fabiato, A. 1985. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine carciac Purkinje cell. J. Gen. Physiol. 85:247–289
Fabiato, A., Fabiato, F. 1979. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J. Physiol. (Paris) 75:463–505
Feldmeyer, D., Melzer, W., Pohl, B. 1990. Effects of gallopamil on calcium release and intramembrane charge movements in frog skeletal muscle fibres. J. Physiol. 421:343–362
Flood, P.R. 1968. Structure of the segmental trunk muscle in Amphioxus. Z. Zellforschung 84:389–416
Flood, P.R. 1977. The sarcoplasmic reticulum and associated plasma membrane of trunk muscle lamellae in Branchiostoma lanceolatum (Pallas). Cell Tissue Res. 181:169–196
Franzini-Armstrong, C. 1975. Membrane particles and transmission at the triad. Fed. Proc. 34:1382–1389
Goll, A., Ferry, D.R., Striessnig J., Schober, M., Glossmann, H. 1984. (−)-[3H]Desmethoxyverapamil, a novel Ca2+ channel probe. FEBS Lett. 176:371–377
Grocki, K. 1982. The fine structure of the deep muscle lamellae and their sarcoplasmic reticulum in Branchiostoma lanceolatum. Eur. J. Cell Biol. 28:202–212
Gurney, A.M., Nerbonne, J.M., Lester, H.A. 1985. Photoinduced removal of nifedipine reveals mechanisms of calcium antagonist action on single heart cells. J. Gen. Physiol. 86:353–379
Hagiwara, S., Henkart, M.P., Kidokoro, Y. 1971. Excitation-contraction coupling in Amphioxus muscle cells. J. Physiol. 219:233–251
Henkart, M., Landis, D.M.D., Reese, T.S. 1976. Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J. Cell. Biol. 70:338–347
Herrmann-Frank, A. 1989. Caffeine- and Ca2+-induced mechanical oscillations in isolated skeletal muscle fibres of the frog. J. Muscle Res. Cell Motil. 10:437–445
Huxley, A.F., Taylor, R.E. 1958. Local activation of striated muscle fibres. J. Physiol. 144:426–441
Ikemoto, N., Ronjat, M., Meszaros, L.G., Koshita, M. 1989. Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry 28:6764–6771
Inui, M., Saito, A., Fleischer, S. 1987. Purification of the ryanodine receptor and identity with the feet structures of terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J. Biol. Chem. 262:1740–1747
Kyhse-Andersen, J. 1984. Electroblotting of multiple gels: A simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10:203–209
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lai, F.A., Erickson, H.P., Block, B.A., Meissner, G. 1987. Evidence for a junctional feet-ryanodine receptor complex from sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 143:704–709
Lai, F.A., Erickson, H.P., Rousseau, E., Liu, Q.Y., Meissner, G. 1988. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331:315–319
Lamb, G.D. 1991. Ca2+ channels or voltage sensors? Nature 352:113
Lamb, G.D., Walsh, T. 1987. Calcium currents, charge movement and dihydropyridine binding in fast- and slow-twitch muscles of rat and rabbit. J. Physiol. 393:595–617
Lüttgau, H.C., Böhle, T., Schnier, A. 1992. Ca2+ antagonists as tools in the analysis of excitation-contraction coupling in skeletal muscle fibres. In: Excitation-Contraction Coupling in Skeletal, Cardiac, and Smooth Muscle. G.B. Frank, C.P. Bianchi, and H. TerKeurs, editors. Plenum, New York (in press)
Lüttgau, H.C., Spiecker, W. 1979. The effects of calcium deprivation upon mechanical and electrophysiological parameters in skeletal muscle fibres of the frog. J. Physiol. 296:411–429
MacLennan, D.H., Brandl, C.J., Korczak, B., Green, N.M. 1985. Aminoacid sequence of a Ca2+ + Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature 316:696–700
MacLennan, D.H., Campbell, K.P., Reithmeier, R.A.F. 1983. Calsequestrin. In: Calcium and Cell Function. A. Martonosi, editor. Vol. 4, pp. 151–173. Academic, New York
Meissner, G., Henderson, J.S. 1987. Rapid calcium release from cardiac sarcoplasmic reticulum vesicles is dependent on Ca2+ and is modulated by Mg2+, adenine nucleotide, and calmodulin. J. Biol. Chem. 262:3065–3073
Melzer, W. 1982a. Electrical membrane properties of the muscle lamellae in Branchiostoma myotomes. Eur. J. Cell Biol. 28:213–218
Melzer, W. 1982b. Twitch activation in Ca2+-free solutions in the myotomes of the lancelet (Branchiostoma lanceolatum). Eur. J. Cell Biol. 28:219–225
Michalak, M., Dupraz, P., Shoshan-Barmatz, V. 1988. Ryanodine binding to sarcoplasmic reticulum membrane; comparison between cardiac and skeletal muscle. Biochim. Biophys. Acta 939:587–594
Morad, M., Goldman, Y.E., Trentham, D.R. 1983. Rapid photochemical inactivation of Ca2+ antagonists shows that Ca2+ entry directly activates contraction in frog heart. Nature 304:635–638
Neuhaus, R., Rosenthal, R., Lüttgau, H.C. 1990. The effects of dihydropyridine derivates on force and Ca2+ current in frog skeletal muscle fibres. J. Physiol. 427:187–209
Pizarro, G., Brum, G., Fill, M., Fitts, R., Rodriguez, M., Uribe, I., Rios, E. 1988. The voltage sensor of skeletal muscle excitation-contraction coupling: A comparison with Ca2+ channels. In: The Calcium Channel: Structure, Function and Implications. M. Morad, W. Nayler, S. Kazda, and M. Schramm, editors. pp. 138–156. Springer-Verlag, Berlin
Rios, E., Pizzaro, G. 1991. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol. Rev. 71:849–907
Scheuer, T., Gilly, W.F. 1986. Charge movement and depolarization-contraction coupling in arthropod vs. vertebrate skeletal muscle. Proc. Natl. Acad. Sci. USA 83:8799–8803
Schneider, M.F., Chandler, W.K. 1973. Voltage dependent charge movement in skeletal muscle: A possible step in excitation-contraction coupling, Nature 242:244–246.
Simon, B.J., Beam, K.G. 1985a. Slow charge movement in mammalian skeletal muscle. J. Gen. Physiol. 85:1–19
Simon, B.J., Beam, K.G., 1985b. The influence of transverse tubular delays on the kinetics of charge movement in mammalian skeletal muscle. J. Gen. Physiol. 85:21–42
Sipido, K.R., Wier, W.G. 1991. Flux of Ca2+ across the sarcoplasmic reticulum of guinea-pig cardiac cells during excitation-contraction coupling. J. Physiol. 435:605–630
Spiecker, W., Melzer, W., Lüttgau, H.Ch. 1979. Extracellular Ca2+ and excitation-contraction coupling. Nature 280: 158–160
Takeshima, H., Nishimura, S., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T., Numa, S. 1989. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339:439–445
Tanabe, T., Beam, K.G., Adams, B.A., Niidome, T., Numa, S. 1990a. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 346:567–569
Tanabe, T., Beam, K.G., Powell, J.A., Numa, S. 1988. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336:134–139
Tanabe, T., Mikami, A., Numa, S., Beam, K.G. 1990b. Cardiactype excitation-coupling in dysgenic skeletal muscle injected with cardiac dihydropyridine receptor cDNA. Nature 344:451–453
Towbin, H., Staehelin, T., Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350–4354
Varsanyi, M., Messer, M., Brandt, N.R., Heilmeyer, L.M.G. Jr. 1986. Phosphatidylinositol 4,5-bisphosphate formation in rabbit skeletal and heart muscle membranes. Biochem. Biophys. Res. Commun. 138:1395–1404
Wray, W., Boulikas, T., Wray, V.P., Handock, R. 1981. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118:197–203
Author information
Authors and Affiliations
Additional information
We thank Drs. H.Ch. Lüttgau and L.M.G. Heilmeyer, Jr. for stimulating discussions during the work, Dr. N.R. Brandt for helpful suggestions, and Drs. A.H. Caswell and M. Michalak for their generous gifts of antibodies. We also thank Ms. P. Goldmann, Mr. R. Schwalm, and Mr. U. Siemen for technical support and Ms. E. Linnepe for editorial help. This work was supported by grant G1 72/1-5 of the Deutsche Forschungsgemeinschaft. R. Benterbusch was recipient of a scholarship by the Studienstiftung des Deutschen Volkes.
Rights and permissions
About this article
Cite this article
Benterbusch, R., Herberg, F.W., Melzer, W. et al. Excitation-contraction coupling in a pre-vertebrate twitch muscle: The myotomes of Branchiostoma lanceolatum . J. Membarin Biol. 129, 237–252 (1992). https://doi.org/10.1007/BF00232906
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00232906