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Myofibrillar proteins in white muscle of the developing African catfish Heterobranchus longifilis (Siluriforms, Clariidae)

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Abstract

Developmental changes in myofibrillar protein composition were investigated in the myotomal muscle of the African catfish, Heterobranchus longifilis (Clariidae), by several electrophoretic techniques. The main muscle fibres of larvae and the fast-white muscle fibres of juvenile and adult fish were found to express distinct myosin heavy chain and myosin light chain 2 (LC2) isoforms. Three myosin LC2 chains were successively detected, differing by their isoelectric points. In contrast, the alkali light chains remained qualitatively and quantitatively unchanged during fish growth. Actin, α-tropomyosin, and troponin-C (TN-C) were also similar in larval, juvenile, and adult white muscle, but an additional larval tropomyosin isoform was found in the first developmental stages. Two isoforms of troponin-T (TN-T) and troponin-I (TN-I) were synthesised in the course of fish growth. Transition from the larval to the adult isoform was much faster for TN-T than for TN-I. Slow-red muscle myofibrils from adult H. longifilis showed no common component (except actin) with larval, juvenile, or adult fast-white muscle myofibrils. Red myofibrils displayed a single TN-T and a single TN-I isoform, but two isoforms of TN-C. The myofibrillar protein isoforms synthesised at any given developmental stage almost certainly reflect changes in the functional requirements of swimming muscles in the course of fish development.

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References

  • Baras, E. 1999. Sibling cannibalism among juvenile vundu under controlled conditions. I. Cannibalistic behaviour, prey selection and prey size selectivity. J. Fish Biol. 54: 82–105.

    Google Scholar 

  • Bassani, V. and Dalla Libera, L. 1991. Myosin isoforms in white, red and pink muscles of the teleost sea bass (Dicentrarchus labrax L.). BAM 1: 153–156.

    Google Scholar 

  • Bone, Q. 1978. Locomotor muscle. In: Fish Physiology. Vol. 7, pp. 361–424. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.

    Google Scholar 

  • Brooks, S. and Johnston, I.A. 1993. Influence of development and rearing temperature on the distribution, ultrastructure and myosin sub-unit composition of myotomal muscle-fibre types in the plaice Pleuronectes platessa. Mar. Biol. 117: 501–513.

    Google Scholar 

  • Campbell, K.P., MacLennan, D.H. and Jorgensen, A.O. 1983. Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye 'stains-all'. J. Biol. Chem. 258: 11267–11273.

    Google Scholar 

  • Chanoine, C., Saadi, A., Guyot-Lenfant, M., Hebbrecht, C. and Gallien, C.L. 1990. Myosin structure in the eel (Anguilla anguilla L.). Demonstration of three heavy chains in adult lateral muscle. FEBS Lett. 277: 200–204.

    Google Scholar 

  • Chanoine, C., Guyot-Lenfant, M., El Attari, A., Saadi, A. and Gallien, C.L. 1992. White muscle differentiation in the eel (Anguilla anguilla L.): changes in the myosin isoforms pattern and ATPase profile during post-metamorphic development. Differentiation 49: 69–75.

    Google Scholar 

  • Chikou, A., Huriaux, F., Laleye, P., Vandewalle, P. and Focant, B. 1997. Isoform distribution of parvalbumins and of some myofibrillar proteins in adult and developing Chrysichthys auratus (Geoffroy St Hilaire, 1808) (Pisces, Claroteidae). Arch. Physiol. Biochem. 105: 611–617.

    Google Scholar 

  • Crockford, T. and Johnston, I.A. 1993. Developmental changes in the composition of myofibrillar proteins in the swimming muscles of Atlantic herring, Clupea harengus. Mar. Biol. 115: 15–22.

    Google Scholar 

  • Crockford, T., Wommack, K.E., Johnston, I.A., McAndrew, B.J., Mutungi, G. and Johnson, T.P. 1991. Inter-and intra-specific variation in myosin light chain and troponin I composition in fast muscle fibres from two species of fish (Genus Oreochromis) which have different temperature-dependent contractile properties. J. Muscle Res. Cell Motil. 12: 439–446.

    Google Scholar 

  • Danieli Betto, D., Zerbato, E. and Betto, R. 1986. Type I, 2A and 2B myosin heavy chain electrophoretic analysis of rat muscle fibers. Biochem. Biophys. Res. Commun. 138: 981–987.

    Google Scholar 

  • Focant, B. and Huriaux, F. 1976. Light chains of carp and pike skeletal muscle myosins. Isolation and characterization of the most anodic light chain on alkaline pH electrophoresis. FEBS Lett. 65: 16–19.

    Google Scholar 

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

    Google Scholar 

  • Focant, B., Huriaux, F., Vandewalle, P., Castelli, M. and Goessens, G. 1992. Myosin, parvalbumin and myofibril expression in barbel (Barbus barbus L.) lateral white muscle during development. Fish Physiol. Biochem. 10: 133–143.

    Google Scholar 

  • Focant, B., Vandewalle, P. and Huriaux, F. 1994. Myosin polymorphism during the development of the trout, Oncorhynchus mykiss. Arch. Int. Physiol. Biochim. Biophys. 102: B54.

    Google Scholar 

  • Focant, B., Mélot, F., Collin, S., Vandewalle, P. and Huriaux, F. 1996. Distribution of myosin and parvalbumin isoforms during the development of the catfish. Arch. Physiol. Biochem. 104: B18.

    Google Scholar 

  • Focant, B., Mélot, F., Collin, S., Chikou, A., Vandewalle, P. and Huriaux, F. 1999. Muscle parvalbumin isoforms of Clarias gariepinus, Heterobranchus longifilis and Chrysichthys auratus: isolation, characterization, and expression during development. J. Fish Biol. 54: 832–851.

    Google Scholar 

  • Gillis, J.M. and Gerday, Ch. 1977. Calcium movements between myofibrils, parvalbumins and sarcoplasmic reticulum in muscle. In: Calcium-binding Proteins and Calcium Function. pp. 193–196. Edited by R.H. Wasserman, R.A. Corradino, E. Carafoli, R.H. Kretsinger, D.H. MacLennan and F.L. Siegel. Elsevier, Amsterdam, North-Holland.

    Google Scholar 

  • Hecht, T., Oellermann, L. and Verheust, L. 1996. Perspectives on clariid culture in Africa. In: The Biology and Culture of Catfishes. Edited by M. Legendre and J.-P. Proteau. Aquat. Living Resour. 9 Special Issue: 197–206.

  • Heeley, D.H. and Hong, C. 1994. Isolation and characterization of tropomyosin from fish muscle. Comp. Biochem. Physiol. 108B: 95–106.

    Google Scholar 

  • Heeley, D.H., Bieger, T., Waddleton, D.M., Hong, C., Jackman, D.M., McGowan, C., Davidson, W.S. and Beavis, R.C. 1995. Characterization of fast, slow and cardiac muscle tropomyosins from salmonid fish. Eur. J. Biochem. 232: 226–234.

    Google Scholar 

  • Huriaux, F. and Focant, B. 1977. Isolation and characterization of the three light chains from carp white muscle myosin. Arch. Int. Physiol. Biochim. 85: 917–929.

    Google Scholar 

  • Huriaux, F. and Focant, B. 1985. Electrophoretic and immunological study of myosin light chains from freshwater teleost fishes. Comp. Biochem. Physiol. 82B: 737–743.

    Google Scholar 

  • Huriaux, F. Vandewalle, P., Philippart, J.C. and Focant, B. 1990. Electrophoretic comparison of myosin light chains and parvalbumins of trunk and head muscles from two barbel (Barbus barbus) populations. Comp. Biochem. Physiol. 97B: 547–553.

    Google Scholar 

  • Huriaux, F., Vandewalle, P. and Focant, B. 1991. Myosin heavy chain isoforms in white, red and ventricle muscles of barbel (Barbus barbus L.). Comp. Biochem. Physiol. 100B: 309–312.

    Google Scholar 

  • Huriaux, F., Mélot, F., Vandewalle, P., Collin, S. and Focant, B. 1996. Parvalbumin isotypes in white muscle from three teleost fish: characterization and their expression during development. Comp. Biochem. Physiol. 113B: 475–484.

    Google Scholar 

  • Huriaux, F., Collin, S., Vandewalle, P., Philippart, J.C. and Focant, B. 1997. Characterization of parvalbumin isotypes in white muscle from the barbel and expression during development. J. Fish Biol. 50: 821–836.

    Google Scholar 

  • James, R.S., Cole, N.J., Davies, M.L.F. and Johnston, I.A. 1998. Scaling of intrinsic contractile properties and myofibrillar protein composition of fast muscle in the fish Myoxocephalus scorpius L. J. Exp. Biol. 201: 901–912.

    Google Scholar 

  • Johnston, I.A., Davison, W. and Goldspink, G. 1977. Energy metabolism of carp swimming muscles. J. Comp. Physiol. 114: 203–216.

    Google Scholar 

  • Johnston, I.A., Cole, N.J., Viera, V.L.A. and Davidson, I. 1997. Temperature and developmental plasticity of muscle phenotype in herring larvae. J. Exp. Biol. 200: 849–868.

    Google Scholar 

  • Karasinski, J. 1993. Diversity of native myosin and myosin heavy chain in fish skeletal muscles. Comp. Biochem. Physiol. 106B: 1041–1047.

    Google Scholar 

  • Karasinski, J. and Kilarski, W. 1989. Polymorphism of myosin isoenzymes and myosin heavy chains in histochemically typed skeletal muscles of the roach (Rutilus rutilus L., Cyprinidae, Fish). Comp. Biochem. Physiol. 92B: 727–731.

    Google Scholar 

  • Koumans, J.T.M. and Akster, H.A. 1995. Myogenic cells in development and growth of fish. Comp. Biochem. Physiol. 110A: 3–20.

    Google Scholar 

  • Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, Lond. 227: 680–685.

    Google Scholar 

  • Legendre, M. and Teugels, G.G. 1991. Développement et tolérance à la température des œufs de Heterobranchus longifilis, et comparaison des développements larvaires de H.longifilis et de Clarias gariepinus (Teleostei, Clariidae). Aquat. Living Resour. 4: 227–240.

    Google Scholar 

  • Legendre, M., Teugels, G.G., Cauty, C. and Jalabert, B. 1992. A comparative study on morphology, growth rate and reproduction of Clarias gariepinus (Burchell, 1822), Heterobranchus longifilis Valenciennes, 1840, and their reciprocal hybrids (Pisces, Clariidae). J. Fish Biol. 40: 59–79.

    Google Scholar 

  • Martinez, I. Ofstad, R. and Olsen, R.L. 1990. Myosin isoforms in red and white muscles of some marine teleost fishes. J. Muscle Res. Cell Motil. 11: 489–495.

    Google Scholar 

  • Martinez, I. Christiansen, J.S., Ofstad, R. and Olsen, R.L. 1991. Comparison of myosin isoenzymes present in skeletal and cardiac muscles of the Arctic charr Salvelinus alpinus (L.). Sequential expression of different myosin heavy chains during development of the fast white skeletal muscle. Eur. J. Biochem. 195: 743–753.

    Google Scholar 

  • Martinez, I., Bang, B., Hatlen, B. and Blix, P. 1993. Myofibrillar proteins in skeletal muscles of parr, smolt and adult Atlantic salmon (Salmo salar L.). Comparison with another salmonid, the Arctic charr Salvelinus alpinus (L.). Comp. Biochem. Physiol. 106B: 1021–1028.

    Google Scholar 

  • Martinez, I. and Christiansen, J.S. 1994. Myofibrillar proteins in developing white muscle of the Arctic charr, Salvelinus alpinus (L.) Comp. Biochem. Physiol. 107B: 11–20.

    Google Scholar 

  • McCubbin, W.D., Oikawa, K., Sykes, B.D. and Kay, C.M. 1982. Purification and characterization of troponin C from pike muscle: a comparative spectroscopic study with rabbit skeletal muscle troponin C. Biochemistry 21: 5948–5956.

    Google Scholar 

  • Moss, R.L., Giulian, G.G. and Greaser, M.L. 1982. Physiological effects accompanying the removal of myosin LC2 from skinned skeletal muscle fibers. J. Biol. Chem. 257: 8588–8591.

    Google Scholar 

  • O'Farrell, P.H. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250: 4007–4021.

    Google Scholar 

  • O'Farrell, P.Z., Goodman, H.M. and O'Farrell, P.H. 1977. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12: 1133–1141.

    Google Scholar 

  • Otémé, Z., Hem, J.S. and Legendre, M. 1996. Nouvelles espèces de poissons-chats pour le développement de la pisciculture africaine. In: The Biology and Culture of Catfishes. Edited by M. Legendre and J.-P. Proteau. Aquat. Living Resour. 9 Special Issue: 207–217.

  • Pette, D. and Staron, R.S. 1990. Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev. Physiol. Biochem. Pharmacol. 116: 1–76.

    Google Scholar 

  • Pires, E., Perry, S.V. and Thomas, M.A.W. 1974. Myosin light-chain kinase, a new enzyme from striated muscle. FEBS Lett. 41: 292–296.

    Google Scholar 

  • Rowlerson, A., Scapolo, P.A., Mascarello, F., Carpenè, E. and Veggetti, A. 1985. Comparative study of myosins present in the lateral muscle of some fish: species variations in myosin isoforms and their distribution in red, pink and white muscle. J. Muscle Res. Cell Motil. 6: 601–640.

    Google Scholar 

  • Scapolo, P.A., Veggetti, A., Mascarello, F. and Romanello, M.G. 1988. Developmental transitions of myosin isoforms and organisation of the lateral muscle in the teleost Dicentrarchus labrax (L.). Anat. Embryol. 178: 287–295.

    Google Scholar 

  • Schiaffino, S. and Reggiani, C. 1996. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol. Rev. 76: 371–423.

    Google Scholar 

  • Schleicher, M. and Watterson, D.M. 1983. Analysis of differences between Coomassie blue stain and silver stain procedures in polyacrylamide gels: conditions for the detection of calmodulin and troponin C. Anal. Biochem. 131: 312–317.

    Google Scholar 

  • Sender, P.M. 1971. Muscle fibrils: solubilization and gel electrophoresis. FEBS Lett. 17: 106–110.

    Google Scholar 

  • Syska, H., Perry, S.V. and Trayer, I.P. 1974. A new method of preparation of troponin I (inhibitory protein) using affinity chromatography. Evidence for three different forms of troponin I in striated muscle. FEBS Lett. 40: 253–257.

    Google Scholar 

  • Vandekerckhove, J. and Weber, K. 1984. Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. J. Mol. Biol. 179: 391–413.

    Google Scholar 

  • Vandewalle, P., Gluckmann, I., Baras, E., Huriaux, F. and Focant, B. 1997. Postembryonic development of the cephalic region in Heterobranchus longifilis. J. Fish Biol. 50: 227–253.

    Google Scholar 

  • Weatherley, A.H. and Gill, H.S. 1985. Dynamics of increase in muscle fibers in fishes in relation to size and growth. Experientia 41: 353–354.

    Google Scholar 

  • Yancey, P.H. and Johnston, I.A. 1982. Effect of electrical stimulation and exercise on the phosphorylation state of myosin light chains from fish skeletal muscle. Pflügers Arch. 393: 334–339.

    Google Scholar 

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Huriaux, F., Vandewalle, P., Baras, E. et al. Myofibrillar proteins in white muscle of the developing African catfish Heterobranchus longifilis (Siluriforms, Clariidae). Fish Physiology and Biochemistry 21, 287–301 (1999). https://doi.org/10.1023/A:1007835101472

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