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Morphometry of muscle fibre types in the carp (Cyprinus carpio L.)

Relationships between structural and contractile characteristics

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Summary

Ultrastructural parameters of muscle fibre types of the carp (Cyprinus carpio L.) were measured and compared with their contractile properties. In red fibres, which are slower than pink fibres, the relative length of the junction between the T system and the sarcoplasmic reticulum (T-SR junction) is smaller and the Z lines are thicker than in pink fibres. Pink fibres have a smaller relative length of T-SR junction than white fibres from the axial muscles. The two types of red fibres present in carp muscle also differ in their relative lengths of T-SR junction. Significant differences in the relative areas of the SR were not found.

The relative volume of myofibrils in red fibres is two-thirds that in pink fibres, a difference that is not reflected in the maximal isometric tetanic tensions of these types. Red fibres, which are less easily fatigued than pink fibres, have larger relative volumes of subsarcolemmal and intermyofibrillar mitochondria. Small pink fibres have a larger relative volume of subsarcolemmal mitochondria than large pink fibres, but have a similar relative volume of intermyofibrillar mitochondria. Small and large pink fibres differ in the relative volumes of their membrane systems, but have similar relative lengths of T-SR junction.

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References

  • Akster HA (1981) Ultrastructure of muscle fibres in head and axial muscles of the perch (Perca fluviatilis L.). A quantitative study. Cell Tissue Res 219:111–131

    Google Scholar 

  • Akster HA (1983) A comparative study of fibre type characteristics and terminal innervation in head and axial muscle of the carp (Cyprinus carpio L.): A histochemical and electron-microscopical study. Neth J Zool 33:164–188

    Google Scholar 

  • Akster HA, Osse JWM (1978) Muscle fibre types in head muscles of the perch Perca fluviatilis (L), Teleostei. A histochemical and electromyographical study. Neth J Zool 28:94–110

    Google Scholar 

  • Akster HA, Granzier HLM, ter Keurs HEDJ (1985) A comparison of quantitative ultrastructural and contractile characteristics of muscle fibre types of the perch, Perca fluviatilis. L. J Comp Physiol (in press)

  • Barets A (1961) Contribution a l'étude des systèmes moteurs “lent” et “rapide” du muscle latéral des téléostéens. Arch Anat Morphol Exp 50 (Suppl):91–187

    Google Scholar 

  • Bone Q (1978) Locomotor muscle. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic Press, New York, vol VII:361–424

    Google Scholar 

  • Briggs FN, Poland JL, Solaro RJ (1977) Relative capabilities of sarcoplasmic reticulum in fast and slow mammalian skeletal muscles. J Physiol 266:587–594

    Google Scholar 

  • Celio MR, Heizmann CW (1982) Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature 297:504–506

    Google Scholar 

  • Cullen MJ, Hollingworth S, Marshall MW (1984) A comparative study of the transverse tubular system of the rat extensor digitorum longus and soleus muscles. J Anat 138:297–308

    Google Scholar 

  • Egginton S, Johnston IA (1982) A morphometric analysis of regional differences in myotomal muscle ultrastructure in the juvenile eel (Anguilla anguilla L). Cell Tissue Res 222:579–596

    Google Scholar 

  • Eisenberg BR, Eisenberg RS (1982) The T-SR junction in contracting single skeletal muscle fibers. J Gen Physiol 79:1–19

    Google Scholar 

  • Eisenberg BR, Kuda AM (1975) Stereological analysis of mammalian skeletal muscle. II. White vastus muscle of the adult Guinea Pig. J Ultrastruct Res 51:176–187

    Google Scholar 

  • Eisenberg BR, Kuda AM (1976) Discrimination between fiber populations in mammalian skeletal muscle by using ultrastructural parameters. J Ultrastruct Res 54:76–88

    Google Scholar 

  • Eisenberg BR, Salmons S (1981) The reorganisation of subcellular structure in muscle undergoing fast-to-slow type transformation. A Stereological study. Cell Tissue Res 220:449–471

    Google Scholar 

  • Eisenberg BR, Kuda AM, Peter JB (1974) Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig. J Cell Biol 60:732–754

    Google Scholar 

  • Fawcett DW, Revel JP (1961) The sarcoplasmic reticulum of a fast-acting fish muscle. J Biophys Biochem Cytol 10, Suppl 4:89–104

    Google Scholar 

  • Flitney FW (1971) The volume of the T-system and its association with the sarcoplasmic reticulum in slow muscle fibres of the frog. J Physiol 217:243–257

    Google Scholar 

  • Focant B, Huriaux F, Johnston IA (1976) Subunit composition of fish myofibrils: the light chains of myosin. Int J Biochem 7:129–133

    Google Scholar 

  • Focant B, Jacob MF, Huriaux F (1981) Electrophoretic comparison of the proteins of some perch (Perca fluviatilis L) head muscles. J Musc Res Cell Motil 2:295–305

    Google Scholar 

  • Focant B, Huriaux F, Vandewalle P (1983) Electrophoretic differentiation of the fibre types of the adductor mandibulae, sternohyoideus and protractor hyoideus muscles of the carp (Cyprinus carpio L). Comp Biochem Physiol 76B:283–289

    Google Scholar 

  • Franzini-Armstrong C (1970) Studies of the triad. I. Structure of the junction in frog twitch fibers. J Cell Biol 47:488–499

    Google Scholar 

  • Franzini-Armstrong C (1973) Membranous systems in muscle fibers. In: Bourne GH (ed) The structure and function of muscle. Academic Press, New York, London, vol II:532–620

    Google Scholar 

  • Gauthier GF (1979) Ultrastructural identification of muscle fiber types by immunocytochemistry. J Cell Biol 82:391–400

    Google Scholar 

  • Gerday C, Gillis JM (1976) The possible role of parvalbumins in the control of contraction. J Physiol 258:96P

  • Gillis JM, Thomason D, Lefèvre J, Kretsinger RH (1982) Parvalbumins and muscle relaxation: a computer simulation study. J Musc Res Cell Motil 3:377–398

    Google Scholar 

  • Granzier HLM, Wiersma J, Osse JWM, Akster HA, van Dommelen WMCM (1982) Contractile properties of a white- and a red-fibre type of the m. hyohyoideus of the carp (Cyprinus carpio L). J Musc Res Cell Motil 3:122

    Google Scholar 

  • Granzier HLM, Wiersma J, Akster HA, Osse JWM (1983) Contractile properties of a white- and a red-fibre type of the m. hyohyoideus of the carp (Cyprinus carpio L). J Comp Physiol 149:441–449

    Google Scholar 

  • Green HJ, Klug GA, Reichmann H, Seedorf U, Wiehrer W, Pette D (1984) Exercise-induced fibre type transitions with regard to myosin, parvalbumin and sarcoplasmic reticulum in muscles of the rat. Pflügers Arch 400:432–438

    Google Scholar 

  • Hagiwara S, Takahashi K (1967) Resting and spike potentials of skeletal muscle fibres of salt-water elasmobranch and teleost fish. J Physiol 190:499–518

    Google Scholar 

  • Hamoir G, Focant B, Distèche M (1972) Proteinic criteria of differentiation of white, cardiac and various red muscles in carp. Comp Biochem Physiol 41B:665–674

    Google Scholar 

  • Hamoir G, Gerardin-Otthiers N, Focant B (1980) Protein differentiation of the superfast swimbladder muscle of the toadfish Opsanus tau. J Mol Biol 143:155–160

    Google Scholar 

  • Hamoir G, Gerardin-Otthiers N, Grodent V, Vandewalle P (1981) Sarcoplasmic differentiation of head muscles of the carp Cyprinus carpio (Pisces, Cypriniformes). Mol Physiol 1:45–58

    Google Scholar 

  • Heilmann C, Pette D (1979) Molecular transformations in sarcoplasmic reticulum of fast-twitch muscle by electro-stimulation. Eur J Biochem 93:437–446

    Google Scholar 

  • Heilmann C, Brdiczka D, Nickel E, Pette D (1977) ATPase activities, Ca2+ transport and phosphoprotein formation in sarcoplasmic reticulum subfractions of fast and slow rabbit muscles. Eur J Biochem 81:211–222

    Google Scholar 

  • Heizmann CW (1984) Parvalbumin, an intracellular calcium-binding protein; distribution, properties and possible roles in mammalian cells. Exp 40:910–920

    Google Scholar 

  • Hess A (1970) Vertebrate slow muscle fibres. Physiol Rev 50:40–62

    Google Scholar 

  • Huriaux F, Lefebvre F, Focant B (1983) Myosin polymorphism in muscles of the toadfish, Opsanus tau. J Musc Res Cell Motil 4:223–232

    Google Scholar 

  • Johnston IA (1982) Biochemistry of myosins and contractile properties of fish skeletal muscle. Mol Physiol 2:15–29

    Google Scholar 

  • Johnston IA, Davison W, Goldspink G (1977) Energy metabolism of carp swimming muscles. J Comp Physiol B 114:203–216

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137a-138a

    Google Scholar 

  • Kilarski W, Kozłowska M (1983) Ultrastructural characteristic of the teleostean muscle fibers and their nerve endings. The stickleback (Gasterosteus aculeatus L). Z mikrosk-anat Forsch Leipzig 97:1022–1036

    Google Scholar 

  • Kim DH, Witzmann FA, Fitts RH (1981) A comparison of sarcoplasmic reticulum function in fast and slow skeletal muscle using crude homogenate and isolated vesicles. Life Sci 28:2223–2229

    Google Scholar 

  • Klug G, Reichmann H, Pette D (1983a) Rapid reduction in parvalbumin concentration during chronic stimulation of rabbit fast twitch muscle. FEBS Lett 152:180–182

    Google Scholar 

  • Klug G, Wiehrer W, Reichmann H, Leberer E, Pette D (1983b) Relationships between early alterations in parvalbumins, sarcoplasmic reticulum and metabolic enzymes in chronically stimulated fast twitch muscle. Pflügers Arch 399:280–284

    Google Scholar 

  • Kronnie G te, Pool CW, Scholten G, Van Raamsdonk W (1980) Myofibrillar differences among mammalian skeletal muscle fibres at the ultrastructural level. A comparison of immunocytochemical and morphological parameters. Eur J Cell Biol 22:780–788

    Google Scholar 

  • Kronnie G te, Tatarczuch L, van Raamsdonk W, Kilarski W (1983) Muscle fibre types in the myotome of stickleback, Gasterosteus aculeatus L; a histochemical, immunohistochemical and ultrastructural study. J Fish Biol 22:303–316

    Google Scholar 

  • Kryvi H (1977) Ultrastructure of the different fibre types in axial muscles of the sharks Etmopterus spinax and Galeus melastomus. Cell Tissue Res 184:287–300

    Google Scholar 

  • Kubišta V, Kubštová J, Pette D (1971) Thyroid hormone induced changes in the enzyme activity pattern of energy-supplying metabolism of fast (white), slow (red), and heart muscle of the rat. Eur J Biochem 18:553–560

    Google Scholar 

  • Mathias RT, Levis RA, Eisenberg RS (1980) Electrical models of excitation-contraction coupling and charge movement in skeletal muscle. J Gen Physiol 76:1–31

    Google Scholar 

  • McArdle HJ, Johnston IA (1981) Ca2+-uptake by tissue sections and biochemical characteristics of sarcoplasmic reticulum isolated from fish fast and slow muscles. Eur J Cell Biol 25:103–107

    Google Scholar 

  • Miledi R, Parker I, Zhu PH (1983) Calcium transients studied under voltage-clamp control in frog twitch muscle fibres. J Physiol 340:649–680

    Google Scholar 

  • Miledi R, Parker I, Zhu PH (1984) Extracellular ions and excitation-contraction coupling in frog twitch muscle fibres. J Physiol 351:687–710

    Google Scholar 

  • Müller W (1976) Subsarcolemmal mitochondria and capillarization of soleus muscle fibers in young rats subjected to an endurance training. A morphometric study of semithin sections. Cell Tissue Res 174:367–389

    Google Scholar 

  • Nag AC (1972) Ultrastructure and adenosine triphosphatase activity of red and white muscle fibers of the caudal region of a fish, Salmo gairdneri. J Cell Biol 55:42–57

    Google Scholar 

  • Nakajima Y (1669) Fine structure of red and white muscle fibres and their neuromuscular junctions in the snake fish (Ophio cephalus argus). Tissue and Cell 1:229–246

    Google Scholar 

  • Page SG (1965) A comparison of the fine structures of frog slow and twitch muscle fibres. J Cell Biol 26:477–497

    Google Scholar 

  • Page SG (1968) Fine structure of tortoise skeletal muscle. J Physiol 197:709–715

    Google Scholar 

  • Page SG (1979) Structure and some contractile properties of fast and slow muscles of the chicken. J Physiol 205:131–145

    Google Scholar 

  • Page SG, Huxley HE (1963) Filament length in striated muscle. J Cell Biol 19:369–390

    Google Scholar 

  • Patterson S, Goldspink G (1972) The fine structure of red and white myotomal muscle fibres of the coalfish (Gadus virens). Z Zellforsch 133:463–474

    Google Scholar 

  • Pool CW, van Raamsdonk W, Diegenbach PC, Mijzen P, Schenkkan EJ, van der Stell A (1976) Muscle fibre typing with sera against myosin and actin. A comparison between enzyme- and immunohistochemical classification. Acta Histochem 57:20–33

    Google Scholar 

  • Salmons S, Gale DR, Sréter FA (1978) Ultrastructural aspects of the transformation of muscle fibre type by long term stimulation: changes in Z discs and mitochondria. J Anat 127:17–31

    Google Scholar 

  • Schneider MF, Chandler WK (1973) Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–246

    Google Scholar 

  • Sitte H (1967) Morphometrische Untersuchungen an Zellen. In: Weibel ER, Elias H (eds) Quantitative methods in morphology. Springer, New York, pp 167–197

    Google Scholar 

  • Slinde E, Kryvi H (1980) Studies on the nature of the Z-discs in skeletal muscle fibres of sharks Etmopterus spinax L and Galeus melastomus Rafinesque-Schmaltz. J Fish Biol 16:299–308

    Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. WH Freeman and Company, San Francisco

    Google Scholar 

  • Somlyo AV (1979) Bridging structures spanning the junctional gap at the triad of skeletal muscle. J Cell Biol 80:743–750

    Google Scholar 

  • Sréter FA (1969) Temperature, pH and seasonal dependence of Ca-uptake and ATPase activity of white and red muscle microsomes. Arch Biochem Biophys 134:25–33

    Google Scholar 

  • Takeuchi A (1959) Neuromuscular transmission of fish skeletal muscles investigated with intracellular microelectrodes. J Cell Comp Physiol 54:211–220

    Google Scholar 

  • Van Raamsdonk W, te Kronnie G, Pool CW, van de Laarse W (1980) An immune histochemical and enzymic characterization of the muscle fibres in myotomal muscle of the teleost Brachydanio rerio, Hamilton-Buchanan. Acta Histochem 67:200–216

    Google Scholar 

  • Van Raamsdonk W, van 't Veer L, Veeken K, Heyting C, Pool CW (1982) Differentiation of muscle fiber types in the teleost Brachydanio rerio, the zebrafish. Posthatching development. Anat Embryol 164:51–62

    Google Scholar 

  • Van Winkle WB, Schwartz A (1978) Morphological and biochemical correlates of skeletal muscle contractility in the cat. I. Histochemical and electron microscopic studies. J Cell Physiol 97:99–119

    Google Scholar 

  • Van Winkle WB, Entman ML, Bornet EP, Schwartz A (1978) Morphological and biochemical correlates of skeletal muscle contractility in the cat. II. Physiological and biochemical studies. J Cell Physiol 97:121–135

    Google Scholar 

  • Weibel ER, Bolender RP (1973) Stereological techniques for electron microscopic morphometry. In: Hayat MA (ed) Principles and techniques of electron microscopy. Van Nostrand Reinhold Company, New York, pp 237–296

    Google Scholar 

  • Wiehrer W, Pette D (1983) The ratio between intrinsic 115 kDa and 30 kDa peptides as a marker of fibre type-specific sarcoplasmic reticulum in mammalian muscles. Febs Lett 158:317–320

    Google Scholar 

  • Zawadowska B, Kilarski W (1983) Muscle fibre composition of the eye muscles of the carp (Cyprinus carpio L) defined on the base of histochemical observations. Folia Histochem Cytochem 21:115–126

    Google Scholar 

  • Zubrzycka-Gaarn E, Korczak B, Osinska H, Sarzala MG (1982) Studies on sarcoplasmic reticulum from slow-twitch muscle. J Musc Res Cell Motil 3:191–212

    Google Scholar 

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  1. Department of Experimental Animal Morphology and Cell Biology, Agricultural University, Wageningen, The Netherlands

    Hendrica A. Akster

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Akster, H.A. Morphometry of muscle fibre types in the carp (Cyprinus carpio L.). Cell Tissue Res. 241, 193–201 (1985). https://doi.org/10.1007/BF00214641

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