Abstract
Effects of exercise on the distribution of phosphofructokinase (PFK), fructose-1,6-biphosphatase (FBPase), and AMP-deaminase between free and particulate-bound fractions was analyzed in white skeletal muscle of rainbow trout Oncorhynchus mykiss. With a widely used technique for the separation of free and bound enzyme fractions (homogenization in low ionic strength, high sucrose buffer), the data showed that the amount of bound PFK increased from 64 to 95% during burst swimming whereas other enzymes were unaffected. Since this data for AMP-deaminase contrasted with earlier reports, different methods of separating free and bound enzyme were evaluated. A clear effect of exercise on AMP-deaminase binding occurred when high ionic strength media (either KCl or KF) were used; in extraction media containing 150 mM KCl, the percent bound rose from 30% in controls to 97% after 1 min burst swimming. Exercise also produced stable changes to AMP-deaminase kinetic properties, including for the bound enzyme (compared with the free) a 2-fold higher Km AMP, a 3-fold higher Ki for inorganic phosphate, and a 60% increase in Ka ADP after 1 min burst exercise. The data suggest that AMP-deaminase in working skeletal muscle is subject to combined controls by allosteric effectors, post-translational modification, and distribution between free and bound states.
Similar content being viewed by others
References cited
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
Brooks, S.P.J. 1992. A simple computer program with statistical tests for the analysis of enzyme kinetics. BioTechniques 13: 906–911.
Brooks, S.P.J. and Storey, K.B. 1988a. Subcellular enzyme binding in glycolytic control: in vivo studies with fish muscle. Am. J. Physiol. 255: R289–R294.
Brooks, S.P.J. and Storey, K.B. 1988b. Reevaluation of the “glycolytic complex” in muscle: a multitechnique approach using trout white muscle. Arch. Biochem. Biophys. 267: 13–22.
Brooks, S.P.J. and Storey, K.B. 1991a. Where is the glycolytic complex? A critical evaluation of present data from muscle tissue. FEBS Lett. 278: 135–138.
Brooks, S.P.J. and Storey, K.B. 1991b. A quantitative evaluation of the effect of enzyme complexes on the glycolytic rate in vivo: mathematical modeling of the glycolytic complex. J. Theor. Biol. 149: 361–375.
Brooks, S.P.J. and Storey, K.B. 1993. Control of metabolic rate by multienzyme complexes: is glycolysis in hypoxia and anoxia regulated by complex formation? In Surviving Hypoxia: Mechanisms of Control and Adaptation. pp. 281–293. Edited by P.W. Hochachka, P.L. Lutz, T.J. Sick M. Rosenthal and G. van den Thillart. CRC Press, Boca Raton.
Clarke, F.M., Shaw, F.D. and Morton, D.J. 1980. Effect of electrical stimulation post-mortem of bovine muscle on the binding of glycolytic enzymes. Biochem. J. 186: 105–109.
Clarke, F.M., Stephan, P., Huxham, G., Hamilton, D. and Morton, D.J. 1984. Metabolic dependence of glycolytic enzyme binding in rat and sheep heart. Eur. J. Biochem. 138: 643–649.
Duncan, J.A. and Storey, K.B. 1991. Role of enzyme binding in muscle metabolism of the goldfish. Can. J. Zool. 69: 1571–1576.
Duncan, J.A. and Storey, K.B. 1992. Subcellular enzyme binding and the regulation of glycolysis in anoxic turtle brain. Am. J. Physiol. 262: R517–R523.
Ferguson, R.A. and Storey, K.B. 1992. Gluconeogenesis in trout (Oncorhynchus mykiss) white muscle: purification and characterization of fructose- 1,6-bisphosphatase activity in vitro. Fish Physiol. Biochem. 10: 201–212, 1992.
Hultin, H.O. 1975 Effect of environment on kinetic characteristics of chicken lactate dehydrogenase isozymes. In Isozymes II, Physiology and Function, pp. 69–85. Edited by C.L. Markert. Academic Press, New York.
Johnston, I.A. 1981. Structure and function of fish muscle. Symp. Zool. Soc. London, 48: 71–113.
Kaletha, K., Thebault, M. and Raffin, J.-P. 1991. Comparative studies on heart and skeletal muscle AMP-deaminase from rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 99 B: 751–754.
Kurganov, B.I. 1986. The role of multienzyme complexes in integration of cellular metabolism. J. Theor. Biol. 119: 445–455.
Lushchak, V.I. 1992a. Free and membrane-bound lactate dehydrogenase from white driving muscles of skate. Biochem. Int. 26: 905–912.
Lushchak, V.I. 1992b. Interaction of lactate dehydrogenase with cellular structures: possible physiological implications. Biokhimiya (Russia) 57: 1142–1154.
Luther, M.A. and Lee, J.C. 1986. The role of phosphorylation in the interaction of rabbit muscle phosphofructokinase with F-actin. J. Biol. Chem. 261: 1753–1759.
Mommsen, T.P. and Hochachka, P.W. 1988. The purine nucleotide cycle as two temporally separated metabolic units: a study on trout muscle. Metabolism 37: 552–556.
Parkhouse, W.S., Dobson, G.P. and Hochachka, P.W. 1988. Control of glycogenolysis in rainbow trout muscle during exercise. Can. J. Zool. 66: 345–351.
Parkhouse, W.S., Dobson, G.P., Belcastro, A.N. and Hochachka, P.W. 1987. The role of intermediary metabolism in the maintenance of proton and charge balance during exercise. Mol. Cell. Biochem. 77: 37–47.
Rahim, Z.H.A., Lutaya, G. and Griffiths, J.R. 1979. Activation of AMP aminohydrolase during skeletal-muscle contraction. Biochem. J. 184: 173–176.
Roberts, S.J., Lowery, M.S. and Somero, G.N. 1988. Regulation of binding of phosphofructokinase to myofibrils in the red and white muscle of the barred sand bass Paralabrax nebulifer (Serranidae). J. Exp. Biol. 137: 13–27.
Rundell, K.W., Tullson, P.C. and Terjung, R.L. 1993. AMP-deaminase binding in rat skeletal muscle after high-intensity running. J. Appl. Physiol. 74: 2004–2006.
Schulte, P.M., Moyes, C.D. and Hochachka, P.W. 1992. Integrating metabolic pathways in post-exercise recovery of white muscle. J. Exp. Biol. 166: 181–195.
Shiraki, H., Miyamoto, S., Matsuda, Y., Momose, E. and Nakagawa, H. 1981. Possible correlation between binding of muscle type AMP-deaminase to myofibrils and ammoniagenesis in rat skeletal muscle on electrical stimulation. Biochem. Biophys. Res. Commun. 100: 1099–1103.
Shiraki, H., Ogawa, H., Matsuda, Y. and Nakagawa, H. 1979a. Interaction of rat muscle AMP-deaminase with myosin. I. Biochemical study of the interaction of AMP-deaminase and myosin in rat muscle. Biochim. Biophys. Acta. 566: 335–344.
Shiraki, H., Ogawa, H., Matsuda, Y. and Nakagawa, H. 1979b. Interaction of rat muscle AMP-deaminase with myosin. II. Modification of the kinetic and regulatory properties of rat muscle AMP-deaminase by myosin. Biochim. Biophys. Acta. 566: 345–352.
Smiley, K.L., Berry, A.J. and Suelter, C.H. 1967. An improved purification, crystallization and some properties of rabbit muscle 5′-adenylic acid deaminase. J. Biol. Chem. 242: 2502–2506.
Storey, K.B. 1991. Metabolic consequences of exercise in organs of rainbow trout. J. Exp. Zool. 260: 157–164.
Su, Y. and Storey, K.B. 1992. Phosphofructokinase from white muscle of the rainbow trout, Oncorhynchus mykiss: purification and properties. Biochim. Biophys. Acta. 1160: 3001–3008.
Thakkar, J.K., Janero, D.R., Yarwood, C. and Sharif, H.M. 1993. Modulation of mammalian cardiac AMP-deaminase by protein kinase C-mediated phosphorylation. Biochem. J. 291: 523–527.
Thillart, G. van den, Waarde, A. van, Muller H.J., Erkelens, C., Addink, A. and Lugtenburg, J. 1989. Fish muscle energy metabolism measured by in vivo 31P-NMR during anoxia and recovery. Am. J. Physiol. 256: R922–R929.
Tovmasian, E.K., Hairapetian, R.L., Bykova, E.V., Severin, S.E. and Haroutunian, A.V. 1990. Phosphorylation of the skeletal muscle AMP-deaminase by protein kinase C. FEBS Lett. 259: 321–323.
Waarde, A. van and Kesbeke, F. 1981. Regulatory properties of AMP-deaminase from lateral red muscle and dorsal white muscle of goldfish, Carassius auratus (L.). Comp. Biochem. Physiol. 69 B: 413–423.
Wokoma, A. and Johnston, I.A. 1983. Anaerobic metabolism during activity in rainbow trout (Salmo gairdneri). Experientia 39: 1366–1367.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lushchak, V.I., Storey, K.B. Influence of exercise on the distribution of enzymes in trout white muscle and kinetic properties of AMP-deaminase from free and bound fractions. Fish Physiol Biochem 13, 407–418 (1994). https://doi.org/10.1007/BF00003420
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00003420