Summary
The trunk muscle lamellae of Amphioxus is made up of cross-striated lamellae about 1 μm thick. Transverse tubules are absent, but numerous subsarcolemmal vesicles are found in both tissue blocks and minced samples after aldehyde and osmium fixation, embedding and sectioning.
The vesicles contain a granular matrix, range in diameter from 30 to 200 nm and constitute about 3 to 6% of the muscle fibre volume. 8 out of 10 vesicles are found above the Z and I-bands. In the presence of oxalate, electron dense precipitates form within the vesicles. Energy-dispersive X-ray microanalysis reveals the presence of Calcium in these precipitates.
The area of the plasma membrane is about 2 μm2/μm3 muscle fibre volume. The corresponding area of sarcoplasmic membrane is ca. 1 μm2/μm3. About 20% of the plasma membrane is directly overlaid and coupled to the sarcoplasmic vesicles.
A thin surface coat is present all over the lamellae, but ruthenium red staining indicates that the coat is slightly concentrated above the sarcoplasmic vesicles.
Freeze-fracture replicas reveal tightly packed coarse granular material in the vesicular membrane and less concentrated and smaller particles in the plasma membrane. The latter particles are seen somewhat less commonly above the vesicles than on the rest of the plasma membrane. Likewise, direct replicas of lamella spread on glass slides and freeze-dried, reveal a distinct pattern in the surface coat or its underlying structures, corresponding to the Z and I-bands.
In the scanning electron microscope the general arrangement of the sarcoplasmic vesicles could be examined. In addition, numerous defects in the plasma- and vesicular membranes indicate a strong adhesion between the two.
It is concluded that the trunk muscle lamellae of Amphioxus have a sarcoplasmic reticulum consisting of subsarcolemmal vesicles with calcium sequestrating properties at Z and I-level. Further that the plasma membrane and its surface coat is probably specialized above the vesicles as compared to the rest of the surface.
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References
Berrill, N.J., Sheldow, H.: The fine structure of the connections between muscle cells in ascidian tadpole larva. J. Cell Biol. 23, 664–669 (1964)
Bertaud, W.S., Ryans, D.G., Simpson, F.O.: Freeze-etch studies on fish skeletal muscle. J. Cell Sci. 6, 537–557 (1970)
Bone, Q., Flood, P.R., Mackie, G.O., Singla, C.L.:On the organization of the sarcotubular system in the caudal muscle cells of larvaceans (Tunicata). (In preparation 1977)
Bone, Q., Ryan, K.P.: The structure and innervation of the locomotor muscle of salps (Tunicata; Thaliacea). J. mar. Biol. Ass. U.K. 53, 873–883 (1973)
Branton, D.: Freeze-etching studies of membrane structure. Phil. Trans. B 261, 133–138 (1971)
Bullivant, S.: Freeze-etching and freeze-fracturing. In: Advanced techniques in biological electron microscopy (J.K. Koehler, ed.), pp. 67–112. Berlin-Heidelberg-New York: Springer 1973
Cavey, M.J., Cloney, R.A.: The structure and differentiation of ascidian muscle. Differentiated caudal musculature of Distaplia occidentalis tadpoles. J. Morph. 138, 349–874 (1972)
Chiarandini, D.J., Reuben, J.P., Brandt, P.W., Grundfest, H.: Effect of caffeine on crayfish muscle fibres. I. Activation of contraction and induction of Ca-spike electrogenesis. J. gen. Physiol. 55, 640–664 (1970)
Costantin, L.L., Franzini-Armstrong, C., Podolsky, R.J.: Localization of calcium-accumulating structures in striated muscle fibers. Science 147, 158–160 (1965)
De Meis, L., Hasselbach, W., Machado, R.D.: Characterization of calcium oxalate and calcium phosphate deposits in sarcoplasmic reticulum vesicles. J. Cell Biol. 62, 505–509 (1974)
Diculescu, L, Popescu, L.M., Ionescu, N., Butucescu, N.: Ultrastructural study of calcium distribution in cardiac muscle cells. Z. Zellforsch. 121, 181–198 (1971)
Ebashi, S.: Excitation contraction coupling. Ann Rev. Physiol. 38 (1976)
Ebashi, S., Endo, M., Ohtsuki, I.: Control of muscle contraction. Quart. Rev. Biophys. 2, 351–384 (1969)
Flood, P.R.: The effect of different fixatives on mitochondrial ultrastructure in Amphioxus muscle (Abstract). J. Ultrastruct. Res. 18, 228 (1967)
Flood, P.R.: Structure of the segmental trunk muscle in Amphioxus. With notes on the course and “endings” of the socalled ventral root fibres. Z. Zellforsch. 84, 389–314 (1968)
Flood, P.R.: The sarcoplasmic reticulum of Amphioxus trunk muscle (Abstract). J. Ultrastruct. Res. 29, 569 (1969)
Flood, P.R.: Dry-fracturing techniques for the study of soft internal biological tissues in the scanning electron microscope. In: Scanning electron microscopy, 1975 (O. Johari and I. Corvin, eds.), pp. 287–294. Chicago: IIT Res. Inst. 1975a
Flood, P.R.: Fine structure of the notochord of Amphioxus. Symp. Zool. Soc. Lond. 36, 81–104 (1975b)
Franzini-Armstrong, C.: Studies of the triad I. Structure of the junction in frog twitch fibres. J. Cell Biol. 47, 488–499 (1970)
Franzini-Armstrong, C.: Membranous systems in muscle fibres. In: The structure and function of muscle (G.H., Bourne ed.) 2 ed., Vol.2, pp. 531–619. New York: Acad. Press 1973
Franzini-Armstrong, C.: Freeze fracture of skeletal muscle from the tarantula spider. Structural differentiations of sarcoplasmic reticulum and transverse tubular system membranes. J. Cell Biol. 61, 501–513 (1974)
Hagiwara, S., Henkart, M.P., Kidokoro, Y.: Excitation-contraction coupling in Amphioxus muscle cells. J. Physiol. (Lond.) 219, 233–251 (1971)
Hagiwara, S., Kidokoro, Y.: Na and Ca component of action potential in Amphioxus muscle cells. J. Physiol. (Lond.) 219, 217–232 (1971)
Hagiwara, S., Nakajima, S.: Differences in Na and Ca spikes as examined by application of tetrodotoxin, procain and manganese ions. J. gen. Physiol. 49, 793–806 (1966)
Hagiwara, S., Takahashi, K., Junge, D.: Excitation-contraction coupling in a barnacle muscle fiber as examined with voltage clamp technique. J. gen. Physiol. 51, 157–175 (1968)
Haksar, A., Maudsley, D.V., Péron, F.G., Bedigian, E.: Lanthanum, inhibition of ACTH-stimulated cyclic AMP and corticosterone synthesis in isolated rat adrenocortical cells. J. Cell Biol. 68, 142–153 (1976)
Hall, T.A., Gupta, B.L.: Beam-induced loss of organic mass under electron microprobe conditions. J. Microscopy 100, 177–188 (1974)
Hasselbach, W.: Relaxation and the sarcotubular calcium pump. Fed. Proc. 23, 909–912 (1964)
Hellam, D.C., Podolsky, R.J.: The relation between calcium concentration and isometric force in skinned frog muscle fibers (Abstract). Fed. Proc. 25, 466 (1966)
Helle, K.B., Lønning, S.: Sarcoplasmic reticulum in the portal vein heart and ventricle of the cyclostome Myxine glutinosa (L). J. Molec. Cell Cardiol. 5, 433–439 (1973)
Heumann, H.-G.: Calciumakkumulierende Strukturen in einem glatten Wirbellosenmuskel. Protoplasma 67, 111–115 (1969)
Heuser, J.E., Reese, T.S., Landis, D.M.D.: Functional changes in frog neuromuscular junctions studied with freeze fracture. J. Neurocytol. 3, 109–131 (1974)
Ishikawa, H., Fukuda, Y., Yamada, E.: Freeze-replica observations on frog sartorius muscle. I. sarcolemmal specializations. J. Electron Microscopy 24, 97–107 (1975)
Jewett, P.H., Sommer, J.H., 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: its ultrastructure and the electrophysiological implications of its geometry. J. Cell Biol. 33, 103–129 (1967)
Karnovsky, M.J., Revel, J.P.: Hexagonal pattern in tight junctions as revealed by neutral lanthanum suspensions. J. Cell Biol. 31, 56A-57A (1966)
Kelly, D.E.: The fine structure of skeletal muscle triad junctions. J. Ultrastruct. Res. 29, 37–49 (1969)
Kidokoro, Y., Hagiwara, S., Henkart, M.P.: Electrical properties of obliquely striated muscle fibre membrane of Anodonta glochidium. J. comp. Physiol. 90, 321–338 (1974)
Komnick, H.: Histochemische Calcium-Lokalisation in der Skelettmuskulatur des Frosches. Histochemie 18, 24–29 (1969)
Kryvi, H.: On the presence of sarcoplasmic reticulum in obliquely striated muscles from Sabella penicillum (Polychaeta). J. submicr. Cytol. 5, 23–28 (1973)
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.: Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat. Rec. 171, 347–368 (1971a)
Luft, J.H.: Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat. Rec. 171, 369–416 (1971b)
Martinez-Paloma, A.: The surface coats of animals cells. Int. Rev. Cytol. 29, 29–75 (1970)
McCallister, L.P., Hadek, R.: The localization of calcium in skeletal muscle: its distribution in muscles in which the caffeine-induced contracture was arrested. J. Ultrastruct. Res. 45, 59–81 (1973)
McCallister, L.P., Mumaw, V.R., Munger, B.L.: Stereo ultrastructure of cardiac membrane systems in the rat heart. In: Scanning electron microscopy, 1974 (O. Johari and I. Crovin, eds.), pp. 712–719. Chicago: ITT Res. Inst. 1974
Mill, P.J., Knapp, M.F.: The fine structure of obliquely striated body wall muscles in the earthworm, Lumbricus terrestris. Linn. J. Cell Sci. 7, 233–261 (1970)
Moor, H.: Etching and related problems. In: Freeze-etching. Techniques and applications (E.L. Benedetti and P. Favard, eds.), pp. 21–26. Paris: Soc. Franc. Micr. Electronique 1973
Myklebust, R., Dalen, H., Saetersdal, T.S.: A comparative study in the transmission electron microscope and scanning electron microscope of intracellular structures in sheep heart muscle cells. J. Microscopy 105, 57–65 (1975)
Nakao, T.: An electron microscopic study of the neuromuscular junction in the myotomes of larval lamprey Lanpetra japonica. J. comp. Neurol. 165, 1–16 (1975)
Niedergerke, R.: Movements of calcium in frog heart ventricles at rest and during contractures. J. Physiol. (Lond.) 167, 515–550 (1963a)
Niedergerke, R.: Movements of Ca in beating ventricles of the frog heart. J. Physiol. (Lond.) 167, 551–580 (1963b)
Orkand, R.K.: The relation between membrane potential and contraction in single crayfish muscle fibres. J. Physiol. (Lond.) 161, 143–158 (1962)
Page, S.: Structure of the sarcoplasmic reticulum in vertebrate muscle. Brit. med. Bull. 24, 170–173 (1968)
Peachey, L.D.: Structure of the longitudinal body muscles of Amphioxus. J. biophys. biochem. Cytol. 10, Suppl. 159–176 (1961)
Peachey, L.D.: Structure of the sarcoplasmic reticulum and T-system of striated muscle. Excerpta Med. Internat. Congr. Ser. 87, 388–398 (1965)
Pease, A.C., Jenden, D.J., Howell, J.N.: Calcium uptake in glycerol-extracted rabbit psoas muscle fibres. II Electron microscopic localization of uptake sites. J. cell comp. Physiol. 65, 141–145 (1965)
Peters, A., Mackay, B.: The structure and innervation of the myotomes of the lamprey. J. Anat. (Lond.) 95, 575–585 (1961)
Philips, E.B., Perdue, J.E.: Ultrastructural distribution of cell surface antigens in avian tumor virus-infected chick embryo fibroblasts. J. Cell Biol. 61, 743–756 (1974)
Pinto da Silva, P., Branton, D.: Membrane splitting in freeze-etching. J. Cell Biol. 45, 598–605 (1970)
Podolsky, R.J., Hall, T., Hatchett, S.L.: Identification of oxalate precipitates in striated muscle fibres. J. Cell Biol. 44, 699–702 (1970)
Politoff, A.L., Rose, S., Pappas, G.D.: The calcium binding sites of synaptic vesicles of the frog sartorius neuromuscular junction. J. Cell Biol. 61, 818–823 (1974)
Portzehl, H., Caldwell, P.C., Rüegg, J.C.: The dependence of contraction and relaxation of muscle fibres from the crab Maia squinado on the internal concentration of free calcium ions. Biochim. biophys. Acta (Amst.) 79, 581–591 (1964)
Prosser, C.L.: Comparative animal physiology, 3 ed. 966 pp. Philadelphia: Saunders 1973
Pucci-Minafra, I.: Ultrastructure of muscle cells in Ciona intestinalis tadpoles. A. Embryol. Morph. Exp. 8, 289–305 (1965)
Rash, J.E., Ellisman, M.H.: Studies of excitable membranes. I. Macromolecular specialization of the neuromuscular junction and the nonjunctional sarcolemma. J. Cell Biol. 63, 567–586 (1974)
Rayns, D.G., Simpson, F.O., Bertaud, W.S.: Surface features of striated muscle. I. Guinea pig cardiac muscle. J. Cell Sci. 3, 467–474 (1968)
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, 208–211 (1963)
Rosenblith, J.Z., Ukena, T.E., Yin, H.H., Berlin, R.D., Karnovsky, M.J.: A comparative evaluation of the distribution of concanavalin A-binding sites on the surface of normal, virally transformed and protease-triated fibroblasts. Proc. nat. Acad. Sci. (Wash.) 70, 1625–1629 (1973)
Rosenbluth, J.: Ultrastructure of dyads in muscle fibers of Ascaris lumbricoides. J. Cell Biol. 42, 817–825 (1969)
Saetersdal, T.S., Myklebust, R., Berg Justesen, N.-P.: Ultrastructural localization of calcium in the pigeon papillary muscle as demonstrated by cytochemical studies and X-ray microanalysis. Cell Tiss. Res. 155, 57–74 (1974)
Sandow, A.: Skeletal muscle. Ann. Rev. Physiol. 32, 87–138 (1970)
Sanger, J.W.: Sarcoplasmic reticulum in the cross-striated adductor muscle of the bay scallop Aequipecten irridians. Z. Zellforsch. 118, 156–161 (1971)
Sanger, J.W., McCann, F.V.: Ultrastructure of the myocardium of the moth, Hyalophora cecropia. J. Insect Physiol. 14, 1105–1111 (1968)
Schiaffino, S., Nunzi, M.G., Burighel, P.: T-system in ascidian muscle: organization of the sarcotubular system in the caudal muscle cells of Botryllus schlosseri tadpole larvae. Tiss. Cell. 8, 101–110 (1976)
Schmalbruch, H.: The sarcolemma of skeletal muscle fibres as demonstrated by a replica technique. Cell Tiss. Res. 150, 377–387 (1974)
Somlyo, A.D.: Excitation-contraction coupling in vertebrate smooth muscle: Correlation of ultrastructure with function. Physiologist 15, 338–348 (1972)
Spray, T.L., Waugh, R.A., Sommer, J.R.: Peripheral couplings in adult vertebrate skeletal muscle. Anatomical observations and functional implications. J. Cell Biol. 62, 223–227 (1974)
Steere, R.L.: Freeze-etching techniques and applications. In: Freeze-etching. Techniques and application (E.L. Benedetti and P. Favard, eds.), pp. 233–255. Paris: Soc. Franc. Micr. Electronique 1973
Stolinsky, C., Breathnach, A.S.: Freeze-fracture replication of biological tissues. Techniques, interpretation and Applications. 173 pp. London: Acad. Press 1975
Sybers, H.D., Ashraf, M.: Preparation of cardiac muscle for SEM. In: Scanning electron microscopy, 1973 (O. Johari and I. Corvin, eds.), pp. 341. Chicago: ITT Res. Inst. 1973
Teräväinen, H.: Anatomical and physiological studies on muscles of Lamprey. J. Neurophysiol. 34, 954–973 (1971)
Ukena, T.E., Borysenko, J.Z., Karnovsky, M.J., Berlin, R.D.: Effects of colchicine, cytochalasin B and 2-deoxyglucose on the topographical organization of surface-bound concavalin A in normal and transformed fibroblasts. J. Cell Biol. 61, 70–82 (1974)
Vale, M.G.P., Carvalho, A.P.: Effects of ruthenium red on Ca2+ uptake and ATP-ase of sarcoplasmic reticulum of rabbit skeletal muscle. Biochim. biophys. Acta (Amst.) 325, 29–37 (1973)
Van Steveninck, R.F.M., Van Steveninck, M.E., Hall, T.A., Peters, P.D.: A chlorine-free embedding medium for use in X-ray analytical electron microscope localization of chloride in biological tissues. Histochemie 38, 173–180 (1974)
Watson, M.L.W.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958)
Weibel, E.R., Kistler, G.S., Scherle, W.F.: Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38 (1966)
Weiss, G.B.: Cellular pharmacology of lanthanum. Ann. Rev. Pharmacol. 14, 343–354 (1974)
Yeh, B.K.: Localization of calcium antimonate in the atrial and ventricular fibres of the cat heart. J. Mol. Cell Card. 5, 351–358 (1973)
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I wish to express my sincere gratitude to the directors and staffs at Biologische Anstalt, Helgoland, Laboratoire Arago, Banyuls s. Mer and The Marine Laboratory, Plymouth, for research facilities and supply of material. The staffs at the JEOL application laboratories in London and Paris are acknowledged for their expert assistance with X-ray microanalyses. Further I thank Miss K. Weltzin for type-writing the manuscript, Mr. E.S. Erichsen for skillful preparative work. Mr. R. Haakonsen and Mr. R. Jensen for all photographic work, and Mr. H. Knutsen and Mr. J. Røli for keeping the electron microscopes and the freeze-etching device in excellent working condition. The financial support of the Norwegian Research Council for Science and the Humanities (Grant no. C. 21.30-8) is appreciated
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Flood, P.R. The sarcoplasmic reticulum and associated plasma membrane of trunk muscle lamellae in Branchiostoma lanceolatum (Pallas). Cell Tissue Res. 181, 169–196 (1977). https://doi.org/10.1007/BF00219979
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DOI: https://doi.org/10.1007/BF00219979