Summary
The ascidian myocardium is composed of small striated myoepithelial cells. The sarcoplasmic reticulum (SR) of these cells was reconstructed from serial sections. T-tubules are absent, but subsarcolemmal cisternae of the SR, that may be the counterpart of terminal cisternae, form couplings with the sarcolemma. Longitudinal SR tubules, parallel to the myofilaments, are interconnected near the middle of the A-band and form a transverse collar.
Cinematographic photography of spontaneous contractions in fresh myocardial preparations produced records that could be analyzed frame by frame. Contractions are typically limited to parts of the myofilament field of single cells. They are locally symmetrical with respect to Z-bands; either both A-bands on each side of a Z-band converge on it (contractions), or neither A-band moves with respect to the Z-band.
It is suggested that the spontaneous contractions are the result of local Ca++ release from randomly distributed subsarcolemmal cisternae. It is proposed that the symmetry of contraction is due to a rapid sequestering of Ca++ by the SR collars at the middle of the A-bands and a possible diffusion barrier at that level.
Similar content being viewed by others
References
Baldwin, K. M.: The fine structure and electrophysiology of heart muscle injury. J. Cell biol. 46, 455–476 (1970).
Cloney, R. A., Florey, E.: Ultrastructure of cephalopod chromatophore organs. Z. Zellforsch. 89, 250–280 (1968).
Constantin, L. L., Franzini-Armstrong, C., Podolsky, R.: Localization of calcium-accumulating structures in striated muscle fibers. Science 147, 158–160 (1965).
Ebashi, S., Lipman, F.: Adenosine triphosphate-linked concentration of calcium ions in a particular fraction of rabbit muscle. J. Cell Biol. 14, 389–400 (1962).
Fanburg, B., Finkel, R. M., Martonosi, A.: The role of calcium in the mechanism of relaxation of cardiac muscle. J. biol. Chem. 239, 2298–2306 (1964).
Fawcett, D. W., McNutt, N. S.: The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42, 1–45 (1969).
Flood, P. R.: Structure of the segmental trunk muscle in amphioxus with notes on the course and “endings” of the so-called ventral root fibers. Z. Zellforsch. 84, 398–416 (1968).
Franzini-Armstrong, C.: Sarcolemmal invaginations and the T-system in skeletal muscle fibers. J. Cell Biol. 19, 24A (1963).
Franzini-Armstrong, C.: Studies of the triad. I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47, 488–499 (1970).
Franzini-Armstrong, C.: Studies of the triad. II. Penetration of tracers into the junctional gap. J. Cell Biol. 49, 196–203 (1971).
Gage, P. W., Eisenberg, R. S.: Action potentials, afterpotentials, and excitation-contraction coupling in frog sartorius fibers without transverse tubules. J. gen. Physiol. 53, 298–310 (1969).
Hanson, J., Lowy, J.: The structure of the muscle fibers in the translucent part of the adductor of the oyster, Crassostrea angulata. Proc. roy. Soc. B 154, 173–196 (1961).
Hasselbach, W.: Relaxation and the sarcotubular calcium pump. Fed. Proc. 23, 909–912 (1964).
Hoyle, G.: Interpreting muscle function in invertebrates. Pflügers Arch. ges. Physiol. 291, 12–27 (1966).
Huxley, A. F., Taylor, R. E.: Local activation of striated muscle fibers. J. Physiol. (Lond.) 144, 426–441 (1958).
Huxley, H. E.: Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle. Nature (Lond.) 202, 1067–1071 (1964).
Jewett, P. H., Sommer, J. R., Johnson, E. A.: Cardiac muscle. Its ultrastructure in the finch and hummingbird with special reference to the sarcoplasmic reticulum. J. Cell Biol. 49, 50–65 (1971).
Johnson, E. A., Sommer, J. R.: A strand of cardiac muscle. J. Cell Biol. 33, 103–129 (1967).
Kalk, M.: The organization of a tunicate heart. Tissue Cell 2, 99–118 (1970).
Kelley, A. M.: Sarcoplasmic reticulum and the transverse tubular system in developing rat intercostal muscle. J. Cell Biol. 43, 65a-66a (1969).
Kelley,D., Cahill, M. A.: Skeletal muscle triad junction fine structure; new observations regarding dimples of the sarcoplasmic reticulum terminal cisternae. J. Cell Biol. 43, 66a (1969).
Kisch, B.: The ultrastructure of the myocardium of fishes. Exp. Med. Surg. 24, 220–227 (1966).
Kriebel, M. E.: Electrical characteristics of tunicate heart cell membranes and nexuses. J. gen. Physiol. 52, 46–59 (1968).
Kushmerick, M. J., Podolsky, R. J.: Ionic mobility in muscle cells. Science 166, 1297–1298 (1969).
Legato, M. J., Langer, G. A.: The subcellular localization of calcium ion in mammalian myocardium. J. Cell Biol. 41, 401–423 (1969).
Luft, J. H.: Improvements in epoxy embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Marco, L. A., Nastuk, W. L.: Sarcomeric oscillations in frog skeletal muscle fibers. Science 161, 1357–1358 (1968).
McNutt, N. S., Fawcett, D. W.: The ultrastructure of the cat myocardium. II. Atrial muscle. J. Cell Biol. 42, 46–67 (1969).
Mill, P. J., Knapp, M. F.: The fine structure of obliquely striated muscle in the earthworm Lumbricus terrestris Linn. J. Cell Sci. 7, 233–261 (1970).
Müller, P.: Lokale Kontraktionsauslösung am Herzmuskel. Helv. physiol. pharmacol. Acta 24, C106-C108 (1966).
Niedergerke, R.: Movements of calcium in frog heart ventricles at rest and during contracture. J. Physiol. (Lond.) 167, 515–550 (1963).
Page, E.: Correlations between electron microscope and physiological observations in heart muscle. J. gen. Physiol. 51, 211–220 (1968).
Pasquali-Rouchetti, I.: The organization of the sarcoplasmic reticulum and T-system in the femoral muscle of the houselfy, Musca domestica. J. Cell Biol. 40, 269–272 (1969).
Peachey, L. D.: Structure of the longitudinal body muscles of amphioxus. J. biophys. biochem. Cytol. 10, (Suppl.), 159–176 (1961).
Peachey, L. D.: The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J. Cell Biol. 24, 209–231 (1965).
Porter, K. R.: The sarcoplasmic reticulum: Its recent history and present status. J. Cell Biol. 10 (Suppl.), 219–226 (1961).
Porter, K. R., Palade, G. E.: Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. biophys. biochem. Cytol. 3, 269–300 (1957).
Revel, J. P.: The sarcoplasmic reticulum of the bat cricothyroid muscle. J. Cell Biol. 12, 571–588 (1962).
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Rosenbluth, J.: Obliquely striated muscle. IV. Sarcoplasmic reticulum, contractile apparatus, and endomysium of the body wall muscle of a polychaete, Glycera, in relation to its speed. J. Cell Biol. 36, 245–259 (1968).
Rostgaard, J., Behnke, O.: Fine structural localization of adenine nucleoside phosphatase activity in the sarcoplasmic reticulum and the T-system of rat myocardium. J. Ultrastruct. Res. 12, 579–591 (1965).
Schiaffino, S., Margreth, A.: Coordinated development of the sarcoplasmic reticulum and T-system during postnatal differentiation of rat skeletal muscle. J. Cell Biol. 41, 855–875 (1969).
Smith, D. S.: Reticular organizations within the striated muscle cell. An historical survey of light microscopic studies. J. Cell Biol. 10, (Suppl.), 61–87 (1961).
Smith, P. S.: The organization of flight muscle fibers in the Odonata. J. Cell Biol. 28, 109–126 (1966).
Sommer, J. R., Johnson, E. A.: Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. J. Cell Biol. 36, 497–526 (1968).
Sperelakis, N.: Ultrastructure of the neurogenic heart of Limulus polyphemus. Z. Zellforsch. 116, 443–463 (1971).
Sperelakis, N., Rubio, R., Redick, J.: Sharp discontinuity in sarcomere lengths across intercalated discs of fibrillating cat hearts. J. Ultrastruct. Res. 30, 503–532 (1970).
Staley, N. A., Benson, E. S.: The ultrastructure of frog ventricular muscle and its relationship to mechanisms of excitation-contraction coupling. J. Cell Biol. 38, 99–114 (1968).
Veratti, E.: Investigations on the fine structure of striated muscle fiber. J. Cell Biol. 10 (Suppl.), 1–59 (1961).
Weber, A., Herz, R., Reiss, J.: On the machanism of the relaxing effect of fragmented sarcoplasmic reticulum. J. gen. Physiol. 46, 679–702 (1963).
Weber, A., Herz, R., Reiss, J.: Study of the kinetics of calcium transport by isolated fragmented SR. Biochem. Z. 345, 329–369 (1966).
Winegrad, S.: Intracellular calcium movements of frog skeletal muscle during recovery from tetanus. J. gen. Physiol. 51, 65–83 (1968).
Author information
Authors and Affiliations
Additional information
This investigation was supported in part by an NIH Fellowship (1-F1-GM-40, 488-01) from the National Institute of General Medical Sciences and National Science Foundation Research Grant GB 5394. The authors wish to thank Dr. Albert M. Gordon for his suggestions and stimulating discussion, and for critically reading the manuscript.
Rights and permissions
About this article
Cite this article
Oliphant, L.W., Cloney, R.A. The ascidian myocardium: Sarcoplasmic reticulum and excitation-contraction coupling. Z. Zellforsch 129, 395–412 (1972). https://doi.org/10.1007/BF00307296
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00307296