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Distribution and properties of lactate dehydrogenase isoenzymes in red and white muscle of freshwater fish

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Abstract

The distribution and kinetics of LDH isoenzymes in red and white muscles of 5 species of salmonids, 4 species of cyprinids and one coregonid species were studied. In all species the white muscles are characterized by the occurrence of only the most cathodic isoenzymes, or groups of isoenzymes. The red muscles contained either the full set of isoenzymes (cyprinids) or a selection in which the anodic forms dominated (salmonids, coregonid). The most striking difference between the two types of muscle was met inCoregonus sp. The temperature profiles of pyruvate affinity are similar in all species of fish studied. On the other hand, Km(pyr) values and degree of pyruvate inhibition are closely related and vary greatly with temperature, with the taxonomic position (and thus biology) of the species, and with electrophoresic mobility of the isoenzyme. Highest affinity and strongest inhibition occurred in the anodic (H4) isoenzymes of cyprinids at low temperature; lowest affinity and zero inhibition in the cathodic isoenzymes (Mα4 → Mβ4) of salmonids and coregonids at high temperature. In salmonids the more recently duplicated loci of the M-group of isoenzymes possess identical Km values at all temperatures, whereas the two older M and H loci differ greatly in this respect. Thus the more recent duplication of LDH loci in salmonids and coregonids may be seen as a mechanism by which the tetramers required for LDH activity can be constructed from more closely related subunits than are provided by the older M and H loci.

Some problems in connection with the determination of the kinetic constants of the lactate oxidase reaction are discussed and it is suggested that an alkaline, pyruvate trapping system provides conditions which are more realistic than those of other assay systems. The Km(lactate) values found are in the biological range and, at 20°C, provide further circumstantial evidence that the red muscles of fish should be capable of oxidizing the lactate produced by the white muscles during strenuous exercise. At 4°C the Km(lactate) values are abnormally high in all muscle preparations and thus are not correlated with the Km(pyruvate) values which are lowest at this temperature.

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References cited

  • Bailey, G.S., Tsuyuki, H. and Wilson, A.C. 1976. The number of genes for lactate dehydrogenase in salmonid fishes. J. Fish. Res. Board Can. 33: 760–767.

    Google Scholar 

  • Bergmeyer, H.U. 1974. Methoden der Enzymatischen Analyse. 3.Aufl. Verlag Chemie, Weinheim/Bergstrasse.

    Google Scholar 

  • Bilinski, E. and Jones, R.E.E. 1972. Oxidation of lactate to carbon dioxide by rainbow trout (Salmo gairdneri). J. Fish. Res. Board Can. 29: 1467–1471.

    Google Scholar 

  • Black, E.C. 1957. Alterations in the blood level of lactic acid in certain salmonid fishes following muscular activity. I. Kamloops trout (Salmo gairdneri). J. Fish. Res. Board Can. 14: 117–134.

    Google Scholar 

  • Bouck, G.R. and Ball, R.C. 1968. Comparative electrophoretic patterns of lactate dehydrogenase in three species of trout. J. Fish. Res. Board Can. 25: 1323–1331.

    Google Scholar 

  • Braekkan, O.R. 1956. Function of red muscle in fish. Nature, Lond. 178: 747–748.

    Google Scholar 

  • Brett, J.R. 1964. The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Board Can. 21: 1183–1226.

    Google Scholar 

  • Brett, J.R. 1972. The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Resp. Physiol. 14: 151–170.

    Google Scholar 

  • Cahn, R., Kaplan, N., Levine, L. and Zwilling, E. 1962. Nature and development of lactate dehydrogenase. Science 136: 962–969.

    Google Scholar 

  • Davie, P.S., Wells, R.M.G. and Tetens, V. 1986. Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isoenzymes. Evidence for increased aerobic capacity of white muscle. J. Exp. Zool. 237: 159–171.

    Google Scholar 

  • DiMichele, L. and Powers, D. 1982. Physiological basis for swimming endurance differences between LDH-B genotypes ofFundulus heteroclitus. Science 216: 1014–1016.

    Google Scholar 

  • Driedzic, W.R. and Hochachka, P.W. 1976. Control of energy metabolism in carp white muscle. Am. J. Physiol. 230: 579–582.

    Google Scholar 

  • Driedzic, W.R. and Kiceniuk, J.W. 1976. Blood lactate levels in free swimming trout (Salmo gairdneri) before and after exercise resulting in fatigue. J. Fish. Res. Board Can. 33: 173–176.

    Google Scholar 

  • Driedzic, W.R., Stewart, J.M. and McNairn, G. 1985. Control of lactate oxidation in fish hearts by lactate oxidase activity. Can. J. Zool. 63: 484–487.

    Google Scholar 

  • Eisenthal, R. and Cornish-Bowden, A. 1974. The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters. Biochem. J. 139: 715–720.

    Google Scholar 

  • Everse, J. and Kaplan, N.O. 1975. Mechanisms of action and biological functions of various dehydrogenase isoenzymes. In Isozymes, Vol. 11, pp. 29–43. Edited by C.L.Markert, Academic Press, New York.

  • Forstner, H., Hinterleitner, S., Mähr, K. and Wieser, W. 1983. Towards a better definition of “metamorphosis” inCoregonus sp.: Biochemical, histological and physiological data. Can. J. Fish. Aquat. Sci. 40: 1224–1232.

    Google Scholar 

  • Frankel, J.S. 1980. Lactate dehydrogenase isoenzymes of the leopard danio,Brachidanio nigrofasciatus: their characterization and ontogeny. Comp. Biochem. Physiol. 67B: 133–137.

    Google Scholar 

  • Hakala, M.T., Glaid, A.J. and Schwert, G.W. 1956. Lactic dehydrogenase. II. Variation of kinetic and equilibrium constants with temperature. J. Biol. Chem. 221: 191–209.

    Google Scholar 

  • Henry, T. and Ferguson, A. 1986. Kinetic studies on the lactate dehydrogenase (LDH-5) isozymes of brown trout,Salmo trutta L. Comp. Biochem. Physiol. 82B: 95–98.

    Google Scholar 

  • Hinterleitner, S., Platzer, U. and Wieser, W. 1986. Development of the activities of oxidative, glycolytic and muscle enzymes during early larval life in three families of freshwater fish. J. Fish Biol., (in press).

  • Hofer, R., Ladurner, H., Gattringer, A. and Wieser, W. 1975. Relationship between the temperature preferenda of fishes, amphibians and reptiles and the substrate affinities of their trypsins. J. Comp. Physiol. 99: 345–355.

    Google Scholar 

  • Hulbert, W.C. and Moon, T.W. 1978. The potential for lactate utilization by red and white muscle of the eel,Anguilla rostrata. L. Can. J. Zool. 56: 128–135.

    Google Scholar 

  • Jones, D.R. 1982. Anaerobic exercise in teleost fish. Can. J. Zool. 60: 1131–1134.

    Google Scholar 

  • Kao, Y.-H., Farley, J. and T.M. 1978. Purification and properties of allelic lactate dehydrogenase isozymes at the B2 locus in rainbow trout,Salmo gairdneri. Comp. Biochem. Physiol. 61B: 507–512.

    Google Scholar 

  • Kaplan, N.O. and Ciotti, M.M. 1961. Evolution and differentiation of dehydrogenases. Ann. N. Y. Acad. Sci. 94: 701–722.

    Google Scholar 

  • Klar, G.T., Stalnaker, C.B. and Farley, T.M. 1979. Comparative physical and physiological performance of rainbow trout,Salmo gairdneri, of distinct lactate dehydrogenase B2 phenotypes. Comp. Biochem. Physiol. 63A: 229–235.

    Google Scholar 

  • Lim, S.T., Kay, R.M. and Bailey, G.S. 1975. Lactate dehydrogenase isozymes of salmonid fish: Evidence for unique and rapid functional divergence of duplicated H4 lactate dehydrogenases. J. Biol. Chem. 250: 1790–1800.

    Google Scholar 

  • Neilands, J.B. 1952. Studies on lactic dehydrogenase of heart. I. Purity, kinetics, and equilibria. J. Biol. Chem. 199: 373–381.

    Google Scholar 

  • Panepucci, L.L.L. de, Schwantes, M.L.B. and Schwantes, A.R. 1984. Loci that encode the lactate dehydrogenase in 23 species of fish belonging to the orders Cypriniformes, Siluriformes and Perciformes: adaptive features. Comp. Biochem. Physiol. 77B: 867–876.

    Google Scholar 

  • Reeves, R.B. 1977. The interaction of body temperature and acid-base balance in ectothermic vertebrates. Ann. Rev. Physiol. 39: 559–586.

    Google Scholar 

  • Rosenberg, M. 1971. Epigenetic control of lactate dehydrogenase subunit assembly. Nature New Biology 230: 12–14.

    Google Scholar 

  • Siciliano, M.J. and Shaw, C.R. 1976. Separation and visualisation of enzymes on gels.In Chromatographic and Electrophoretic Techniques, Vol. 2, 4th ed., pp. 185–209. Edited by I. Smith. W. Heinemann, London.

  • Smit, H., Amelink-Koutstaal, I.M., Vijvetberg, J. and von Vaupel-Klein, J.C. 1972. Oxygen consumption and efficiency of swimming in goldfish. Comp. Biochem. Physiol. 39A: 1–28.

    Google Scholar 

  • Vesell, E.S. 1975. Medical uses of isozymes.In Isozymes II. Physiological Function, pp. 1–28. Edited by C.L. Markert, Academic Press, New York.

    Google Scholar 

  • Whitt, G.S. 1970. Developmental genetics of the lactate dehydrogenase isozymes of fish. J. Exp. Zool. 175: 1–36.

    Google Scholar 

  • Whitt, G.S., Miller, E.T. and Shaklee, J.B. 1973. Developmental and biochemical genetics of lactate dehydrogenase isozymes in fishes.In Genetics and Mutagenesis of Fish, pp. 243–276. Edited by J.H. Schröder, Springer Verlag Berlin, Heidelberg, New York.

    Google Scholar 

  • Wieser, W., Platzer, U. and Hinterleitner, S. 1985. Anaerobic and aerobic energy production of young rainbow trout (Salmo gairdneri) during and after bursts of activity. J. Comp. Physiol. 155B: 485–492.

    Google Scholar 

  • Wieser, W., Koch, F., Drexel, E. and Platzer, U. 1986. “Stress” reactions in teleosts: effects of temperature and activity on anaerobic energy production in roach (Rutilus rutilus L.). Comp. Biochem. Physiol. 83A: 41–45.

    Google Scholar 

  • Wilson, T.L. 1977. Theoretical analysis of the effects of two pH regulation patterns on the temperature sensitivities of biological systems in nonhomeothermic animals. Arch. Biochem. Biophys. 182: 409–419.

    Google Scholar 

  • Wilson, F.R., Champion, M.J., Whitt, G.S. and Prosser, C.L. 1975. Isozyme patterns in tissues of temperature-acclimated fish.In Isozymes, Vol. 2, pp. 193–206. Edited by C.L. Markert. Academic Press, New York.

  • Winer, A.D. and Schwert, G.W. 1958. Lactic dehydrogenase: the influence of pH on kinetics of the reaction. J. Biol. Chem. 231: 1065–1083.

    Google Scholar 

  • Wittenberger, G. 1968. Biologie du chinchard de la Mer Noire (Trachurus Mediterraneus ponticus). XV. Recherches sur le metabolisme d'effort chexTrachurus etGobius. Mar. Biol. 2: 1–4.

    Google Scholar 

  • Wittenberger, G. and Diaciuc, I.U. 1965. Effort metabolism of lateral muscle in carp. J. Fish. Res. Board Can. 22: 1397–1406.

    Google Scholar 

  • Wittenberger, G., Coprean, D. and Morar, L. 1975. Studies in the carbohydrate metabolism of the lateral muscles in carp. (Influence of phloridizin, insulin and adrenaline). J. Comp. Physiol. 101: 161–172.

    Google Scholar 

  • Yancey, P.H.M. and Somero, G.N. 1978. Temperature dependence of intracellular pH. Its role in the conservation of pyruvate apparent Km values of vertebrate lactate dehydrogenases. J. Comp. Physiol. 125: 135–141.

    Google Scholar 

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Authors and Affiliations

  1. Institut für Zoologie, Abteilung Zoophysiologie, Universität Innsbruck, Technikerstraβe 25, A-6020, Innsbruck, Austria

    W. Wieser, R. Lackner, S. Hinterleitner & U. Platzer

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  1. W. Wieser
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  2. R. Lackner
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  3. S. Hinterleitner
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  4. U. Platzer
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Wieser, W., Lackner, R., Hinterleitner, S. et al. Distribution and properties of lactate dehydrogenase isoenzymes in red and white muscle of freshwater fish. Fish Physiol Biochem 3, 151–162 (1987). https://doi.org/10.1007/BF02180417

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