Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1992 Jun 15;284(Pt 3):777–780. doi: 10.1042/bj2840777

Mechanism linking glycogen concentration and glycogenolytic rate in perfused contracting rat skeletal muscle.

P Hespel 1, E A Richter 1
PMCID: PMC1132606  PMID: 1622395

Abstract

The influence of differences in glycogen concentration on glycogen breakdown and on phosphorylase activity was investigated in perfused contracting rat skeletal muscle. The rats were preconditioned by a combination of swimming exercise and diet (carbohydrate-free or carbohydrate-rich) in order to obtain four sub-groups of rats with varying resting muscle glycogen concentrations (range 10-60 mumol/g wet wt.). Pre-contraction muscle glycogen concentration was closely positively correlated with glycogen breakdown over 15 min of intermittent short tetanic contractions (r = 0.75; P less than 0.001; n = 56) at the same tension development and oxygen uptake. Additional studies in supercompensated and glycogen-depleted hindquarters during electrical stimulation for 20 s or 2 min revealed that the difference in glycogenolytic rate was found at the beginning rather than at the end of the contraction period. Phosphorylase alpha activity was approximately twice as high (P less than 0.001) in supercompensated muscles as in glycogen-depleted muscles after 20 s as well as after 2 min of contractions. It is concluded that glycogen concentration is an important determinant of phosphorylase activity in contracting skeletal muscle, and probably via this mechanism a regulator of glycogenolytic rate during muscle contraction.

Full text

PDF
777

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aragón J. J., Tornheim K., Lowenstein J. M. On a possible role of IMP in the regulation of phosphorylase activity in skeletal muscle. FEBS Lett. 1980 Aug 25;117 (Suppl):K56–K64. doi: 10.1016/0014-5793(80)80570-9. [DOI] [PubMed] [Google Scholar]
  2. Berger M., Hagg S. A., Goodman M. N., Ruderman N. B. Glucose metabolism in perfused skeletal muscle. Effects of starvation, diabetes, fatty acids, acetoacetate, insulin and exercise on glucose uptake and disposition. Biochem J. 1976 Aug 15;158(2):191–202. doi: 10.1042/bj1580191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bergström J., Hermansen L., Hultman E., Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967 Oct-Nov;71(2):140–150. doi: 10.1111/j.1748-1716.1967.tb03720.x. [DOI] [PubMed] [Google Scholar]
  4. Bergström J., Hultman E. A study of the glycogen metabolism during exercise in man. Scand J Clin Lab Invest. 1967;19(3):218–228. doi: 10.3109/00365516709090629. [DOI] [PubMed] [Google Scholar]
  5. Chasiotis D. Role of cyclic AMP and inorganic phosphate in the regulation of muscle glycogenolysis during exercise. Med Sci Sports Exerc. 1988 Dec;20(6):545–550. [PubMed] [Google Scholar]
  6. Chasiotis D., Sahlin K., Hultman E. Regulation of glycogenolysis in human muscle at rest and during exercise. J Appl Physiol Respir Environ Exerc Physiol. 1982 Sep;53(3):708–715. doi: 10.1152/jappl.1982.53.3.708. [DOI] [PubMed] [Google Scholar]
  7. Conlee R. K., McLane J. A., Rennie M. J., Winder W. W., Holloszy J. O. Reversal of phosphorylase activation in muscle despite continued contractile activity. Am J Physiol. 1979 Nov;237(5):R291–R296. doi: 10.1152/ajpregu.1979.237.5.R291. [DOI] [PubMed] [Google Scholar]
  8. Constable S. H., Favier R. J., Holloszy J. O. Exercise and glycogen depletion: effects on ability to activate muscle phosphorylase. J Appl Physiol (1985) 1986 May;60(5):1518–1523. doi: 10.1152/jappl.1986.60.5.1518. [DOI] [PubMed] [Google Scholar]
  9. DeLange R. J., Kemp R. G., Riley W. D., Cooper R. A., Krebs E. G. Activation of skeletal muscle phosphorylase kinase by adenosine triphosphate and adenosine 3',5'-monophosphate. J Biol Chem. 1968 May 10;243(9):2200–2208. [PubMed] [Google Scholar]
  10. Entman M. L., Keslensky S. S., Chu A., Van Winkle W. B. The sarcoplasmic reticulum-glycogenolytic complex in mammalian fast twitch skeletal muscle. Proposed in vitro counterpart of the contraction-activated glycogenolytic pool. J Biol Chem. 1980 Jul 10;255(13):6245–6252. [PubMed] [Google Scholar]
  11. Galbo H., Holst J. J., Christensen N. J. The effect of different diets and of insulin on the hormonal response to prolonged exercise. Acta Physiol Scand. 1979 Sep;107(1):19–32. doi: 10.1111/j.1748-1716.1979.tb06438.x. [DOI] [PubMed] [Google Scholar]
  12. Gilboe D. P., Larson K. L., Nuttall F. Q. Radioactive method for the assay of glycogen phosphorylases. Anal Biochem. 1972 May;47(1):20–27. doi: 10.1016/0003-2697(72)90274-6. [DOI] [PubMed] [Google Scholar]
  13. Gollnick P. D., Piehl K., Saubert C. W., 4th, Armstrong R. B., Saltin B. Diet, exercise, and glycogen changes in human muscle fibers. J Appl Physiol. 1972 Oct;33(4):421–425. doi: 10.1152/jappl.1972.33.4.421. [DOI] [PubMed] [Google Scholar]
  14. Heilmeyer L. M., Jr, Meyer F., Haschke R. H., Fischer E. H. Control of phosphorylase activity in a muscle glycogen particle. II. Activation by calcium. J Biol Chem. 1970 Dec 25;245(24):6649–6656. [PubMed] [Google Scholar]
  15. Hermansen L., Hultman E., Saltin B. Muscle glycogen during prolonged severe exercise. Acta Physiol Scand. 1967 Oct-Nov;71(2):129–139. doi: 10.1111/j.1748-1716.1967.tb03719.x. [DOI] [PubMed] [Google Scholar]
  16. Hespel P., Richter E. A. Glucose uptake and transport in contracting, perfused rat muscle with different pre-contraction glycogen concentrations. J Physiol. 1990 Aug;427:347–359. doi: 10.1113/jphysiol.1990.sp018175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hickson R. C., Rennie M. J., Conlee R. K., Winder W. W., Holloszy J. O. Effects of increased plasma fatty acids on glycogen utilization and endurance. J Appl Physiol Respir Environ Exerc Physiol. 1977 Nov;43(5):829–833. doi: 10.1152/jappl.1977.43.5.829. [DOI] [PubMed] [Google Scholar]
  18. Jansson E. Diet and muscle metabolism in man with reference to fat and carbohydrate utilization and its regulation. Acta Physiol Scand Suppl. 1980;487:1–24. [PubMed] [Google Scholar]
  19. Jansson E., Hjemdahl P., Kaijser L. Epinephrine-induced changes in muscle carbohydrate metabolism during exercise in male subjects. J Appl Physiol (1985) 1986 May;60(5):1466–1470. doi: 10.1152/jappl.1986.60.5.1466. [DOI] [PubMed] [Google Scholar]
  20. KREBS E. G., LOVE D. S., BRATVOLD G. E., TRAYSER K. A., MEYER W. L., FISCHER E. H. PURIFICATION AND PROPERTIES OF RABBIT SKELETAL MUSCLE PHOSPHORYLASE B KINASE. Biochemistry. 1964 Aug;3:1022–1033. doi: 10.1021/bi00896a003. [DOI] [PubMed] [Google Scholar]
  21. Karlsson J., Saltin B. Diet, muscle glycogen, and endurance performance. J Appl Physiol. 1971 Aug;31(2):203–206. doi: 10.1152/jappl.1971.31.2.203. [DOI] [PubMed] [Google Scholar]
  22. Meinke M. H., Edstrom R. D. Muscle glycogenolysis. Regulation of the cyclic interconversion of phosphorylase a and phosphorylase b. J Biol Chem. 1991 Feb 5;266(4):2259–2266. [PubMed] [Google Scholar]
  23. Meyer F., Heilmeyer L. M., Jr, Haschke R. H., Fischer E. H. Control of phosphorylase activity in a muscle glycogen particle. I. Isolation and characterization of the protein-glycogen complex. J Biol Chem. 1970 Dec 25;245(24):6642–6648. [PubMed] [Google Scholar]
  24. Ren J. M., Broberg S., Sahlin K., Hultman E. Influence of reduced glycogen level on glycogenolysis during short-term stimulation in man. Acta Physiol Scand. 1990 Jul;139(3):467–474. doi: 10.1111/j.1748-1716.1990.tb08948.x. [DOI] [PubMed] [Google Scholar]
  25. Ren J. M., Hultman E. Phosphorylase activity in needle biopsy samples--factors influencing transformation. Acta Physiol Scand. 1988 May;133(1):109–114. doi: 10.1111/j.1748-1716.1988.tb08386.x. [DOI] [PubMed] [Google Scholar]
  26. Rennie M. J., Winder W. W., Holloszy J. O. A sparing effect of increased plasma fatty acids on muscle and liver glycogen content in the exercising rat. Biochem J. 1976 Jun 15;156(3):647–655. doi: 10.1042/bj1560647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Richter E. A., Galbo H., Christensen N. J. Control of exercise-induced muscular glycogenolysis by adrenal medullary hormones in rats. J Appl Physiol Respir Environ Exerc Physiol. 1981 Jan;50(1):21–26. doi: 10.1152/jappl.1981.50.1.21. [DOI] [PubMed] [Google Scholar]
  28. Richter E. A., Galbo H. High glycogen levels enhance glycogen breakdown in isolated contracting skeletal muscle. J Appl Physiol (1985) 1986 Sep;61(3):827–831. doi: 10.1152/jappl.1986.61.3.827. [DOI] [PubMed] [Google Scholar]
  29. Richter E. A., Ruderman N. B., Gavras H., Belur E. R., Galbo H. Muscle glycogenolysis during exercise: dual control by epinephrine and contractions. Am J Physiol. 1982 Jan;242(1):E25–E32. doi: 10.1152/ajpendo.1982.242.1.E25. [DOI] [PubMed] [Google Scholar]
  30. Ruderman N. B., Houghton C. R., Hems R. Evaluation of the isolated perfused rat hindquarter for the study of muscle metabolism. Biochem J. 1971 Sep;124(3):639–651. doi: 10.1042/bj1240639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Soderling T. R., Park C. R. Recent advances in glycogen metabolism. Adv Cyclic Nucleotide Res. 1974;4(0):283–333. [PubMed] [Google Scholar]
  32. Spriet L. L., Berardinucci L., Marsh D. R., Campbell C. B., Graham T. E. Glycogen content has no effect on skeletal muscle glycogenolysis during short-term tetanic stimulation. J Appl Physiol (1985) 1990 May;68(5):1883–1888. doi: 10.1152/jappl.1990.68.5.1883. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES