Summary
Cold acclimation in fish is associated with an elevation in metabolic rate. The present study investigates the role of adenine nucleotides and related compounds in metabolic regulation following temperature acclimation. Brook trout (Salvelinus fontinalis) were acclimated for 10 weeks to either +4°C or +24°C. Both groups of fish were exercised at 2.5 body lengths s−1 for 2 weeks prior to sacrifice in order to control for differences in spontaneous activity.
Concentrations of ATP, ADP, AMP, P i and PC were approximately 2-fold higher in white than red muscles. Temperature acclimation had little effect on total adenine nucleotide concentration in either muscle type. In white fibres acclimation to 4°C results in a 39% increase in [ADP] and [AMP], a 35% decrease in [PC] (phosphorylcreatine), and no significant change in [P i ]. In contrast temperature has little effect on concentrations of these compounds in red muscle.
Parameters of metabolic control — adenylate energy charge ([ATP]+0.5 [ADP]/[ATP]+[ADP]+[AMP]), phosphorylation state ([ATP]/[ADP]·[P i ]), and the ratios [ATP]∶[ADP] and [ATP]∶[AMP] — were significantly lower in cold- than warm-acclimated white muscle. The observed changes in phosphorylation state and [ATP]∶[AMP] are consistent with an increase in mitochondrial respiration and glycolysis, respectively.
In conclusion, changes in metabolites may be an important factor in producing an enhanced metabolic rate in cold-acclimated fish.
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References
Atkinson, D.E.: The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry7, 4030–4034 (1968a)
Atkinson, D.E.: Citrate and the citrate cycle in the regulation of energy metabolism. Biochem. Soc. Symp.27, 23–40 (1968b)
Atkinson, D.E.: Cellular energy metabolism and its regulation. New York: Academic Press 1977
Beis, I., Newsholme, E.A.: The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem. J.152, 23–32 (1975)
Bullock, T.H.: Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. Cambridge Philos. Soc.30, 311–342 (1955)
Cohen, P.: Control of enzyme activity. London: Chapman and Hall 1976
Cohen, P.: The hormonal control of glycogen metabolism in mammalian muscle by multivalent phosphorylation. Biochem. Soc. Trans.7, 459–480 (1979)
Driedzic, W.R., Hochachka, P.W.: Control of energy metabolism in fish white muscle. Am. J. Physiol.230, 579–582 (1976)
Driedzic, W.R., Hochachka, P.W.: Metabolism in fish during exercise. In: Fish physiology, Vol. 7. Hoar, W.S., Randall, D.J. (eds.), pp. 503–544. New York: Academic Press 1978
Erecinska, M., Stubbs, M., Miyata, Y., Ditre, C.M., Wilson, D.F.: Regulation of cellular metabolism by intracellular phosphate. Biochim. Biophys. Acta462, 20–35 (1977)
Fiske, J.H., Subbarow, J.: The colorimetric determination of phosphorus. J. Biol. Chem.66, 375–400 (1925)
Fraser, D.I., Dyer, W.J., Weinstein, H.M., Dingle, J.R., Hines, J.A.: Glycolytic metabolites and their distribution at death in the white and red muscle of cod following various degrees of antemortem activity. Can. J. Biochem.44, 1015–1033 (1966)
Freed, J.M.: Properties of muscle phosphofructokinase of cold- and warm-acclimatedCarassius auratus. Comp. Biochem. Physiol.39B, 747–764 (1971)
Guppy, M., Hulbert, W.C., Hochachka, P.W.: Metabolic sources of heat and power in tuna muscles. II. Enzyme and metabolite profiles. J. Exp. Biol.82, 303–320 (1979)
Guynn, R.W., Veloso, D., Veech, R.L.: Enzymatic determination of inorganic phosphate in the presence of creatine phosphate. Anal. Biochem.45, 277–285 (1972)
Hazel, J.R., Prosser, C.L.: Molecular mechanisms of temperature compensation in poikilotherms. Physiol. Rev.54, 620–677 (1974)
Hazel, J.R., Garlick, W.S., Sellner, P.A.: The effects of assay temperature upon the pH optima of enzymes from poikilotherms: A test of the imidazole alphastal hypothesis. J. Comp. Physiol.123, 97–104 (1978)
Hill, D.K.: The location of adenine nucleotides in the striated muscle of the toad. J. Cell Biol.20, 435–458 (1964)
Hochachka, P.W., Hayes, F.R.: The effect of temperature acclimation on pathways of glucose metabolism in the trout. Can. J. Zool.40, 261–270 (1962)
Jankowsky, H.D.: Versuche zur Adaptation der Fische im normalen Temperaturbereich. Helgol. Wiss. Meeresunters.18, 317–362 (1968)
Jaworek, D., Gruber, W., Bergmeyer, H.U.: Adenosine-5′-triphosphate. Determination with 3-phosphoglycerate kinase. In: Methods of enzymatic analysis, Vol. 4. 2nd edn. Bergmeyer, H.U. (ed.), pp. 2097–2101. Weinheim: Verlag Chemie 1974a
Jaworek, D., Gruber, W., Bergmeyer, H.U.: Adenosine-5′-diphosphate and adenosine-5′-monophosphate. In: Methods of enzymatic analysis, Vol. 4, 2nd ed. Bergmeyer, H.U. (ed.), pp 2127–2131 Weinheim: Verlag Chemie 1974b
Johnston, I.A.: Specialisation of fish muscle. In: Development and specialisation of muscle. Goldspink, D. (ed.) Society of Experimental Biology, Seminar Series Symposium, Cambridge: University Press (in press) 1980
Johnston, I.A., Maitland, B.: Temperature acclimation in Crucian carp: A morphometric analysis of muscle fibre ultrastructure. J. Fish Biol. (in press) 1980
Johnston, I.A., Moon, T.W.: Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J. Comp. Physiol.135, 147–156 (1980a)
Johnston, I.A., Moon, T.W.: Exercise training in skeletal muscles of Brook trout. J. Exp. Biol. (in press) (1980b)
Jones, N.R., Murray, J.: The acid-soluble nucleotides of codling (Godus callarias) muscle. Biochem. J.77, 567–575 (1960)
Künnemann, H., Laudien, H., Precht, H.: Der Einfluß von Temperaturänderungen auf Enzyme der Fischmuskulatur. Versuche mit GoldorfenIdus idus. Mar. Biol.7, 71–81 (1970)
Lamprecht, W., Trautschold, I.: Adenosine-5′-triphosphate — Determination with hexokinase and glucose-6-phosphate dehydrogenase. In: Methods of enzymatic analysis, Vol. 4, 2nd edn. Bergmeyer, H.U. (ed.), pp. 2101–2110. Weinheim: Verlag Chemie 1974
Lännergren, J.: Location of ultraviolet-adsorbing substance in isolated skeletal muscle fibres. The effect of stimulation. J. Physiol. (London)270, 785–800 (1977)
Lehmann, J.: Veranderungen der Enzymaktivitäten nach einen Wechsel der Adaptationstemperatur, untersucht am Seitenrumfplumskel des Goldfisches (Carassius auratus L.). Int. Rev. Fes. Hydrobiol.55, 763–781 (1970)
Longerich, L.L., Feltham, L.A.W.: Changes in muscle phosphofructokinase in temperatur acclimated winter fluonder (Pseudopleuronectus americanus). J. Thermal Biol.3, 61–67 (1978)
Magnall, D., Nesbitt, C.: Studies of the regulation of rabbit muscle phosphofructokinase by the adenine nucleotides. Int. J. Biochem.9, 523–529 (1978)
Newbold, R.P., Scopes, R.K.: Postmortem glycolysis in ox skeletal muscle. Effect of temperature on the concentrations of glycolytic intermediates and cofactors. Biochem. J.105, 127–136 (1967)
Newsholme, E.A.: The role of the fructose 6-phosphate/fructose 1,6-diphosphate cycle in metabolic regulation and heat generation. Biochem. Soc. Trans.4, 978–984 (1976)
Newsholme, E.A., Start, C.: Regulation in metabolism. London: John Wiley and Sons 1973
Newsholme, E.A., Zammit, V.A., Crabtree, B.: The role of glucose and glycogen as fuels for muscle. Biochem. Soc. Trans.6, 512–520 (1978)
Ottaway, J.H., Mowbray, J.: The role of compartmentalisation in the control of glycolysis. In: Current topics in cellular regulation, Vol. 12. Horecker, B.L., Stadtman, E.R. (eds.), pp. 107–207 London: Academic Press 1977
Precht, H., Christophersen, J., Hensel, H., Larcher, W.: Temperature and life. Berlin, Heidelberg, New York: Springer 1973
Pye, V.I., Wieser, W., Zech, M.: The effect of season and experimental temperature on the rates of oxidative phosphorylation of liver and muscle mitochondria from the tench (Tinca tinca). Comp. Biochem. Physiol.54B, 13–20 (1976)
Rahim, Z.H.A., Perrett, D., Griffiths, J.R.: Skeletal muscle purine nucleotide levels in normal and phosphorylase kinase deficient mice. FEBS Lett.69, 203–206 (1976)
Rockstein, M., Herron, P.W.: Colorimetric determination of inorganic phosphate in microgram quantities. Anal. Chem.23, 1500–1501 (1951)
Saito, T., Arai, K.: Further studies on inosinic acid formation in carp muscle. Bull. Jpn. Soc. Sci. Fish.23, 579–583 (1958)
Saito, T., Arai, K., Yajima, T.: Changes in purine nucleotides of red lateral muscles of rainbow trout. Nature (London)184, 1415 (1959)
Seraydarian, K., Mommaerts, W.F.H.M., Wallner, A.: The amount and compartmentalisation of adenosine diphosphate in muscle. Biochim. Biophys. Acta65, 443–460 (1962)
Shen, L.C., Fall, L., Walton, G.M., Atkinson, D.E.: Interaction between energy charge and metabolic modulation in the regulation of enzymes of amphibolic sequences. Phosphofructokinase and pyruvate dehydrogenase. Biochemistry7, 4041–4045 (1968)
Sidell, B.D.: Turnover of cytochromec in skeletal muscle of green sunfish (Lepomis cyanellus R.) during thermal acclimation. J. Exp. Zool.199, 233–250 (1977)
Smit, H., Berg, R.J. Van Den, Kijn-Den Hartog, I.: Some experiments on thermal acclimation in the goldfish (Carassius auratus L.). Neth. J. Zool.24, 32–49 (1974)
Sokal, R.R., Rohlf, F.J.: Biometry. The principles and practice of statistics of biological research. San Francisco: Freeman 1969
Somero, G.N.: Temperature adaptation of enzymes: biological optimisation through structure-function compromises. Annu. Rev. Ecol. Syst.9, 1–29 (1978)
Somero, G.N., Hochachka, P.W.: Isoenzymes and short-term temperature compensation in poikilotherms: activation of lactate dehydrogenase isoenzymes by temperature decreases. Nature (London)223, 194–195 (1969)
Sugden, P.H., Newsholme, E.A.: The effects of ammonium, inorganic phosphate and potassium ions on the activity of phosphofructokinases from muscle and nervous tissues of vertebrates and invertebrates. Biochem. J.150, 113–122 (1975)
Thillart, G. Van Den, Kesbeke, F., Waarde, A. Van: Influence of anoxia on the energy metabolism of goldfish (Carassius auratus L.). Comp. Biochem. Physiol.55A, 329–336 (1976)
Thillart, G. Van Den, Modderkolk, J.: The effect of acclimation temperature on the activation energies of state III respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochim. Biophys. Acta510, 38–51 (1978)
Thillart, G. Van Den, Kesbeke, F., Waarde, A. Van: Anaerobic energy-metabolism of goldfish (Carassius auratus L.). Influence of hypoxia and anoxia on phosphorylated compounds and glycogen. J. Comp. Physiol.136, 45–52 (1980)
Wilson, D.F., Erecinska, M., Dutton, P.L.: Thermodynamic relationships in mitochondrial oxidative phosphorylation. Annu. Rev. Biophys. Bioeng.3, 203–230 (1974)
Wilson, D.F., Owen, C.S., Holian, A.: Control of mitochondrial respiration: a quantitative evaluation of the roles of cytochromec and oxygen. Arch. Biochem. Biophys.182, 749–762 (1977)
Wilson, F.R.: Quantitative changes of enzymes of the goldfish (Carassius auratus L.) in response to temperature acclimation. An immunological approach. Ph. D. thesis, University of Illinois (1973)
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Walesby, N.J., Johnston, I.A. Temperature acclimation in brook trout muscle: Adenine nucleotide concentrations, phosphorylation state and adenylate energy charge. J Comp Physiol B 139, 127–133 (1980). https://doi.org/10.1007/BF00691027
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DOI: https://doi.org/10.1007/BF00691027