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Energy metabolism in the mantle muscle of the squid,Loligo pealeii

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Summary

  1. 1.

    The concentrations of glycolytic and Krebs cycle intermediates, α-glycerophosphate, the adenylates, and free amino acids were determined in the mantle muscle of the squid,Loligo pealeii, at rest and after 10 s of vigorous swimming.

  2. 2.

    Exercise resulted in significant increases in the levels of glucose-6-phosphate, fructose-1,6-diphosphate, and pyruvate. Phosphofructokinase and pyruvate kinase were identified as control points of glycolysis. In the Krebs cycle, changes in the levels of isocitrate and α-ketoglutarate suggested a facilitation of the isocitrate dehydrogenase reaction.

  3. 3.

    The products of anaerobic metabolism in mantle muscle, in particular α-glycerophosphate and octopine, did not accumulate during exercise indicating the aerobic nature of “burst” swimming in these animals.

  4. 4.

    Exercise resulted in a drop in muscle proline concentrations of approximately 2 μmol/g wet wt. which was accompanied by an almost stoichiometric increase in alanine levels.

  5. 5.

    The changes in adenylate concentrations with exercise were dramatic: ATP fell to 39% of the value in resting muscle while ADP and AMP rose 3- and 6-fold, respectively. Arginine phosphate concentrations fell from 10 μmol/g wet wt. in resting to 1 μmol/g wet wt. in exercised muscle.

  6. 6.

    Muscular work in this squid appears to be accompanied by an activation of aerobic carbohydrate metabolism, the α-glycerophosphate cycle functioning to maintain cytoplasmic redox balance. During metabolic activation, the carbon skeleton of proline may be used to augment the pool size of Krebs cycle intermediates. The observed changes in arginine phosphate and AMP levels could be key in the activation of the reactions of glycolysis.

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References

  • 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)

    Google Scholar 

  • Bursell, E.: The conversion of glutamate to alanine in the tsetse fly (Glossina morsitans). Comp. Biochem. Physiol.23, 825–829 (1967)

    Google Scholar 

  • Chance, B., Weber, A.: The steady state of cytochrome B during rest and after contraction in frog sartorius. J. Physiol.169, 263–277 (1963)

    Google Scholar 

  • Drummond, G.I.: Muscle metabolism. Fortschr. Zool.19, 359–429 (1966)

    Google Scholar 

  • Edington, D.W., Ward, G.R., Saville, W.A.: Energy metabolism in working muscle: concentration profiles of selected metabolites. Amer. J. Physiol.224, 1375–1380 (1973)

    Google Scholar 

  • Fields, J., Baldwin, J., Hochachka, P.W.: On the role of octopine dehydrogenase in cephalopod mantle muscle metabolism. Canad. J. Zool.54, 871–878 (1976)

    Google Scholar 

  • Florkin, M.: Nitrogen metabolism. In: Physiology of the mollusca, Vol. II, Ch. 10 (ed. K.M. Wilbur, C.M. Yonge). New York: Academic Press 1966

    Google Scholar 

  • Ghiretti, F.: Respiration. In: Physiology of the mollusca, Vol. II (eds. K.M. Wilbur, C.M. Yonge), pp. 175–208. New York: Academic Press 1966

    Google Scholar 

  • Goudsmit, E.M.: Carbohydrates and carbohydrate metabolism in mollusca. Chem. Zool.7, 219–243 (1972)

    Google Scholar 

  • Grieshaber, M., Gäde, G.: The biological role of octopine in the squid,Loligo vulgaris. J. comp. Physiol.108, 225–232 (1976)

    Google Scholar 

  • Hansford, R.G.: The control of tricarboxylate cycle oxidations in blowfly flight muscle. Biochem. J.142, 509–519 (1974)

    Google Scholar 

  • Hochachka, P.W., Fields, J.H.A., Mustafa, T.: Animal life without oxygen: Basic biochemical mechanisms. Science178, 1056–1060 (1973)

    Google Scholar 

  • Hochachka, P.W., Moon, T.W., Mustafa, T., Storey, K.B.: Metabolic sources of power for mantle muscle of a fast swimming squid. Comp. Biochem. Physiol.52B, 151–158 (1975)

    Google Scholar 

  • Hochachka, P.W., Somero, G.N.: Strategies biochemical adaptation, pp. 67–75. Philadelphia: W.B. Saunders Co. 1973

    Google Scholar 

  • Jobsis, F.: Spectrophotometric studies on intact muscle. J. gen. Physiol.46, 929–937 (1963)

    Google Scholar 

  • Johnson, R.N., Hansford, R.G.: The control of tricarboxylate cycle oxidations in blowfly flight muscle: the steady state concentrations of citrate, isocitrate, 2-oxo-glutarate, and malate in flight muscle and isolated mitochondria. Biochem. J.146, 527–535 (1975)

    Google Scholar 

  • LaNoue, K.F., Bryla, J., Williamson, J.R.: Feedback interactions in the control of citric acid cycle activity in rat heart mitochondria. J. biol. Chem.247, 667–679 (1972)

    Google Scholar 

  • Lowry, O.H., Passonneau, J.V.: A flexible system of enzymic analysis, pp. 146–218. New York: Academic Press 1972

    Google Scholar 

  • Madin, K., Crowe, J.H.: Anhydrobiosis in nematodes; carbohydrate and lipid metabolism during dehydration. J. exp. Zool.193, 335–342 (1975)

    Google Scholar 

  • Moon, T.W., Hulbert, W.C.: The ultrastructure of the mantle musculature of the squid,Symplectoteuthis oualaniensis. Comp. Biochem. Physiol,52B, 145–149 (1975)

    Google Scholar 

  • Neeley, J.R., Rovetto, M.J., Whitmer, J.T., Morgan, H.E.: Effects of ischemia on function and metabolism of the isolated working rat heart. Amer. J. Physiol.225, 651–659 (1973)

    Google Scholar 

  • Piras, R., Staneloni, R.: In vivo regulation of rat muscle glycogen synthetase activity. Biochemistry8, 2153–2160 (1969)

    Google Scholar 

  • Randle, P.J., England, P.J., Denton, R.M.: Control of the tricarboxylate cycle and its interactions with glycolysis during acetate utilization in rat heart. Biochem. J.117, 667–695 (1970)

    Google Scholar 

  • Redfield, A., Goodkind, R.: The significance of the Bohr effect in the respiration and asphyxiation of the squid,Loligo pealeii. Brit. J. exp. Biol.6, 340–349 (1929)

    Google Scholar 

  • Robertson, J.D.: Studies on the chemical composition of muscle tissue. III. The mantel muscle of cephalopod molluscs. J. exp. Biol.42, 153–175 (1965)

    Google Scholar 

  • Rowan, A.: Control of metabolism in locust flight muscle. D. Phil. Thesis, Oxford University (1975)

  • Ruderman, N.B., Berger, M.: The formation of glutamine and alanine in skeletal muscle. J. biol. Chem.249, 5500–5506 (1974)

    Google Scholar 

  • Sacktor, B.: Regulation of intermediary metabolism with special references to control mechanisms in insect flight muscle. Advanc. Insect Physiol7, 267–347 (1970)

    Google Scholar 

  • Sacktor, B., Hurlbert, E.C.: Regulation of metabolism in working muscle in vivo. II. Concentrations of adenine nucleotides, arginine phosphate, and inorganic phosphate in insect flight muscle during flight. J. biol. Chem.241, 632–634 (1966)

    Google Scholar 

  • Sacktor, B., Wormser-Shavit, E.: Regulation of metabolism in working muscle in vivo. I. Concentrations of some glycolytic, tricarboxylic acid cycle, and amino acid intermediates in insect flight muscle during flight. J. biol. Chem.241, 624–631 (1966)

    Google Scholar 

  • Safer, B., Williamson, J.R.: Mitochondrial-cytosolic interactions in perfused rat heart. J. biol. Chem.248, 2570–2579 (1973)

    Google Scholar 

  • Snedecor, G.W., Cochran, W.G.: Statistical methods, 6th ed. Ames, Iowa: Iowa State University Press 1967

    Google Scholar 

  • Storey, K.B.: Purification and properties of squid mantle muscle adenylate kinase J. biol. Chem.251, 7810–7815 (1976)

    Google Scholar 

  • Storey, K.B.: Purification and characterization of arginine kinase from the mantle muscle of the squid. Arch. Biochem. Biophys.179, 518–526 (1977)

    Google Scholar 

  • Storey, K.B., Hochachka, P.W.: Redox regulation of muscle phosphofructokinase in a fast swimming squid. Comp. Biochem. Physiol.52B, 159–164 (1975a)

    Google Scholar 

  • Storey, K.B., Hochachka, P.W.: Alpha-glycerophosphate dehydrogenase: its role in the control of the cytoplasmic arm of the alpha-glycerophosphate cycle in squid muscle. Comp. Biochem. Physiol.52B, 169–174 (1975b)

    Google Scholar 

  • Storey, K.B., Hochachka P.W.: Squid muscle pyruvate kinase: control properties in a tissue with an active alpha-GP cycle. Comp. Biochem. Physiol.52B, 187–192 (1975c)

    Google Scholar 

  • Storey, K.B., Hochachka, P.W.: Squid muscle glyceraldehyde-3-P dehydrogenase: control of the enzyme in a tissue with an active alpha-GP cycle. Comp. Biochem. Physiol.52B, 179–182 (1975d)

    Google Scholar 

  • Veech, R.L., Guynn, R. Veloso, D.: The time course of the effects of ethanol on the redox and phosphorylation state of rat liver. Biochem. J.127, 387–397 (1972)

    Google Scholar 

  • Williamson, J.R.: Glycolytic control mechanisms. II. Kinetics of intermediate changes during the aerobic-anoxic transition in perfused rat heart. J. biol. Chem.241, 5026–5036 (1966)

    Google Scholar 

  • Williamson, J.R.: General features of metabolic control as applied to the erythrocyte. Advanc. biol. Med.6, 117–136 (1970)

    Google Scholar 

  • Williamson, J.R., Corkey, B.E.: Assays of intermediates of the citric acid cycle and related compounds by fluorometric enzyme methods. In: Methods in enzymology, Vol. 13 (ed. J. Lowenstein), pp. 434–513. New York: Academic Press 1969

    Google Scholar 

  • Young, R.E.: A brief review of the biology of oceanic squid,Symplectoteuthis oualaniensis. Comp. Biochem. Physiol.52B, 141–144 (1975)

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, Duke University, 27706, Durham, North Carolina, USA

    Kenneth B. Storey & Janet M. Storey

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  1. Kenneth B. Storey
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  2. Janet M. Storey
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Storey, K.B., Storey, J.M. Energy metabolism in the mantle muscle of the squid,Loligo pealeii . J Comp Physiol B 123, 169–175 (1978). https://doi.org/10.1007/BF00687846

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