Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T08:05:50.221Z Has data issue: false hasContentIssue false
  • English
  • Français

NMR of glycogen in exercise

Published online by Cambridge University Press:  12 June 2007

Thomas B. Price ,
Douglas L. Rothman  and
Robert G. Shulman
Thomas B. Price*
Affiliation:
Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT 06510, USA
Douglas L. Rothman
Affiliation:
Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT 06510, USA
Robert G. Shulman
Affiliation:
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06510, USA
*
*Corresponding Author: Dr Thomas B. Price, fax +1 203 785 6534, email price@boreas.med.yale.edu
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Natural-abundance 13CNMR spectroscopy is a non-invasive technique that enables in vivo assessments of muscle and/or liver glycogen concentrations. Over the last several years, 13C NMR has been developed and used to obtain information about human glycogen metabolism with diet and exercise. Since NMR is non-invasive, more data points are available over a specified time course, dramatically improving the time resolution. This improved time resolution has enabled the documentation of subtleties of muscle glycogen re-synthesis following severe glycogen depletion that were not previously observed. Muscle and liver glycogen concentrations have been tracked in several different human populations under conditions that include: (1) muscle glycogen recovery from intense localized exercise with normal insulin and with insulin suppressed; (2) muscle glycogen recovery in an insulin-resistant population; (3) muscle glycogen depletion during prolonged low-intensity exercise; (4) effect of a mixed meal on postprandial muscle and liver glycogen synthesis. The present review focuses on basic 13C NMR and gives results from selected studies.

Keywords

Muscle metabolismNMRGlycogenExerciseInsulin
Type
Meeting Report
Information
Proceedings of the Nutrition Society , Volume 58 , Issue 4 , November 1999 , pp. 851 - 859
Copyright
The Nutrition Society

References

Avison, MJ, Rothman, DL, Nadel, E, Jue, T & Shulman, RG (1988) Detection of human muscle glycogen by natural abundance 13C NMR. Proceedings of the National Academy of Sciences USA 85, 1634–1636.Google Scholar
Bloch, G, Chase, JR, Meyer, DB, Avison, MJ, Shulman, GI & Shulman, RG (1994) in vivo regulation of rat muscle glycogen resynthesis after intense exercise. American Journal of Physiology 266, E85–E91.Google ScholarPubMed
Constable, SH, Young, JC, Highuchi, M & Holloszy, JO (1984) Glycogen resynthesis in leg muscles of rats during exercise. American Journal of Physiology 247, R880–R883.Google ScholarPubMed
Costill, DL, Gollnick, PD, Jansson, ED, Saltin, B & Stein, EM (1973) Glycogen depletion pattern in human muscle fibres during distance running. Acta Physiologica Scandinavica 89, 374–383.CrossRefGoogle ScholarPubMed
David, M, Petit, WA, Laughlin, MR, Shulman, RG, King, JE & Barrett, EJ (1990) Simultaneous synthesis and degradation of rat liver glycogen. Journal of Clinical Investigation 86, 612–617.Google Scholar
Dietrichson, P, Coakley, J, Smith, PEM, Griffiths, RD, Helliwell, TR & Edwards, RHT (1987) Conchotome and needle percutaneous biopsy of skeletal muscle. Journal of Neurology and Neurosurgery 50, 1461–1467.Google ScholarPubMed
Douen, AG, Ramlal, T, Pastogi, S, Bilan, PJ, Cartee, GD, Vranic, M, Holloszy, JO & Klip, A (1990) Exercise induces recruitment of the ‘insulin-responsive glucose transporter’. Journal of Biological Chemistry 265, 13427–13430.Google Scholar
Gadian, DG, Radda, GK, Richards, RE & Seeley, PJ (1979) P-31 NMR in living tissue: The road from a promising tool to an important tool in biology. In Biological Applications of Magnetic Resonance, pp. 463–536 [Shulman, RG, editor]. New York: Academic Press Inc.Google Scholar
Garetto, LP, Richter, EA, Goodman, MN & Ruderman, NB (1984) Enhanced muscle glucose metabolism after exercise in the rat: the two phases. American Journal of Physiology 246, E471–E475.Google ScholarPubMed
Gollnick, PD, Piehl, K & Saltin, B (1974) Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. Journal of Physiology 241, 45–57.CrossRefGoogle ScholarPubMed
Goodyear, LJ, Hirshman, MF, King, PA, Horton, ED, Thompson, CM & Horton, ES (1990) Skeletal muscle plasma membrane glucose transport and glucose transporters after exercise. Journal of Applied Physiology 68, 193–198.Google Scholar
Gruetter, R, Prolla, TA & Shulman, RG (1991) 13C NMR visibility of rabbit muscle glycogen in vivo. Magnetic Resonance in Medicine 20, 327–332.CrossRefGoogle ScholarPubMed
Harris, RC, Hultman, E & Nordesjo, LO (1974) Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest: Methods and variance of values. Scandinavian Journal of Clinical and Laboratory Investigation 33, 109–120.Google Scholar
Hutber, CA & Bonen, A (1989) Glycogenesis in muscle and liver during exercise. Journal of Applied Physiology 66, 2811–2817.CrossRefGoogle ScholarPubMed
Hwang, JH, Perseghin, G, Rothman, DL, Cline, GW, Magnusson, I, Petersen, KF & Shulman, GI (1995) Impared net hepatic glycogen synthesis in insulin-dependent diabetic subjects during mixed meal ingestion. Journal of Clinical Investigation 95, 783–787.Google Scholar
Ivy, JL, Chi, MM-Y, Hintz, CS, Sherman, WM, Hellendal, RP & Lowry, OH (1987) Progressive metabolite changes in individual human muscle fibers with increasing work rates. American Journal of Physiology 252, C630–C639.Google Scholar
Jue, T, Rothman, DL, Tavitian, BA & Shulman, RG (1989) Natural-abundance 13C NMR study of glycogen repletion in human liver and muscle. Proceedings of the National Academy of Sciences USA 86, 1439–1442.CrossRefGoogle ScholarPubMed
Maehlum, S, Hostmark, AT & Hermansen, L (1977) Synthesis of muscle glycogen during recovery after severe exercise in diabetic and non-diabetic subjects. Scandinavian Journal of Clinical and Laboratory Investigation 37, 309–316.CrossRefGoogle ScholarPubMed
Magnusson, I, Rothman, DL, Gerard, DP, Katz, LD & Shulman, GI (1995) Hepatic glycogenolysis during glucagon infusion in humans. Diabetes 44, 185–189.Google Scholar
Magnusson, I, Rothman, DL, Jucker, B, Shulman, RG & Shulman, GI (1991) 13C NMR studies of liver glycogen turnover in fed and fasted man. Diabetes 40, Suppl., 300.Google Scholar
Pan, JW, Hamm, JR, Rothman, DL & Shulman, RG (1989) In vivo titration of phosphomonoesters by H-1 decoupled P-31 NMR in human skeletal muscle after exercise. Proceedings of the Society of Magnetic Resonance in Medicine Annual Meeting, 542.Google Scholar
Petersen, KF, Price, TB, Cline, GW, Rothman, DL & Shulman, GI (1996) Contribution of net hepatic glycogenolysis to glucose production during the early postprandial period. American Journal of Physiology 270, E186–E191.Google Scholar
Price, TB, Perseghin, G, Duleba, A, Chen, W, Chase, J, Rothman, DL, Shulman, RG & Shulman, GI (1996) NMR studies of muscle glycogen synthesis in insulin resistant offspring of NIDDM parents immediately following glycogen depleting exercise. Proceedings of the National Academy of Sciences USA 93, 5329–5334.CrossRefGoogle ScholarPubMed
Price, TB & Rothman, DL (1999) Tracking human muscle and liver metabolism non-invasively with carbon-13 NMR. In Adaptation Biology and Medicine, Vol. 2, pp. 200–213 [Pandolf, BB, Takeda, N and Singal, PK, editors]. New Dehli, India: Narosa Publishing House.Google Scholar
Price, TB, Rothman, DL, Avison, MJ, Buonamico, P & Shulman, RG (1991) 13C NMR measurements of muscle glycogen during low intensity exercise. Journal of Applied Physiology 70, 1836–1844.CrossRefGoogle ScholarPubMed
Price, TB, Rothman, DL, Taylor, R, Shulman, GI, Avison, MJ & Shulman, RG (1994a) Human muscle glycogen resynthesis after exercise: insulin dependent and independent phases. Journal of Applied Physiology 76, 104–111.CrossRefGoogle ScholarPubMed
Price, TB, Taylor, R, Mason, GM, Rothman, DL, Shulman, GI & Shulman, RG (1994b) Turnover of human muscle glycogen during low-intensity exercise. Medicine and Science in Sports and Exercise 26, 983–991.Google Scholar
Robergs, RA, Pearson, DR, Costill, DL, Fink, WJ, Pascoe, DD, Benedict, MA, Lambert, CP & Zachweija, JJ (1991) Muscle glycogenolysis during differing intensities of weight-resistance exercise. Journal of Applied Physiology 70, 1700–1706.CrossRefGoogle ScholarPubMed
Roch-Norlund, AE, Bergstrom, J & Hultman, E (1972) Muscle glycogen and glycogen synthetase in normal subjects and in patients with diabetes mellitus. Scandinavian Journal of Clinical and Laboratory Investigation 30, 77–84.Google Scholar
Rosetti, L & Giaccan, A (1990) Relative contribution of glycogen synthesis and glycolysis to insulin mediated glucose uptake: a dose response study. Journal of Clinical Investigation 85, 1785–1792.Google Scholar
Rothman, DL, Magnusson, I, Katz, LD, Shulman, RG & Shulman, GI (1990) Quantitation of hepatic glycogenolysis and gluconeogenesis in fasting humans using C-13 NMR. Science 254, 573–576.CrossRefGoogle Scholar
Rothman, DL, Shulman, RG & Shulman, GI (1992) P-31 NMR measurements of muscle glucose-6-phosphate: evidence for reduced insulin dependent muscle glucose transport or phosphorylation in non-insulin dependent diabetes. Journal of Clinical Investigation 89, 1069–1075.Google Scholar
Shulman, GI, Rothman, DL, Chung, Y, Rossetti, L, Petit, WA, Barrett, EJ & Shulman, RG (1988) 13C NMR studies of glycogen turnover in the perfused rat liver. Journal of Biological Chemistry 263, 5027–5029.CrossRefGoogle ScholarPubMed
Shulman, GI, Rothman, DL, Jue, T, Stein, P, DeFronzo, RA & Shulman, RG (1990) Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin dependent diabetes mellitus by 13C nuclear magnetic resonance spectroscopy. New England Journal of Medicine 322, 223–228.Google Scholar
Sillerud, GI & Shulman, RG (1983) Structure and metabolism of mammalian liver glycogen monitored by carbon-13 nuclear magnetic resonance. Biochemistry 22, 1087–1094.Google Scholar
Sternlicht, E, Barnard, RJ & Grimditch, GK (1989) Exercise and insulin stimulate skeletal muscle glucose transport through different mechanisms. American Journal of Physiology 256, E227–E230.Google Scholar
Taylor, R, Magusson, I, Rothman, DL, Cline, GW, Caumo, A, Cobelli, C & Shulman, GI (1996) Direct assessment of liver glycogen storage by 13C nuclear magnetic resonance spectroscopy and regulation of glucose homeostasis after a mixed meal in normal subjects. Journal of Clinical Investigation 97, 126–132.Google Scholar
Taylor, R, Price, TB, Katz, LD, Shulman, RG & Shulman, GI (1993) Direct measurement of change in muscle glycogen concentration after a mixed meal in normal subjects. American Journal of Physiology 265, E224–E229.Google Scholar
Taylor, R, Price, TB, Rothman, DL, Shulman, RG & Shulman, GI (1992) Validation of 13C NMR measurement of human skeletal muscle glycogen by direct biochemical assay of needle biopsy samples. Magnetic Resonance in Medicine 27, 13–20.CrossRefGoogle ScholarPubMed
Vollestad, NK & Blom, PCS (1985) Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiologica Scandinavica 125, 395–405.Google Scholar
Wallberg-Henriksson, H, Constable, SH, Young, DA & Holloszy, JO (1988) Glucose transport into rat skeletal muscle: interaction between exercise and insulin. Journal of Applied Physiology 65, 909–913.Google Scholar
Young, AA, Bogardus, C, Stone, K & Mott, DM (1988) Insulin responses of components of whole-body and muscle carbohydrate metabolism in humans. American Journal of Physiology E231–E236.Google Scholar
Zang, L-H, Laughton, MR, Rothman, DL & Shulman, RG (1990a) 13C NMR relaxation times of hepatic glycogen in vitro and in vivo. Biochemistry 29, 6815–6820.Google Scholar
Zang, L-H, Rothman, DL & Shulman, RG (1990b) 1H NMR visibility of mammalian glycogen in solution. Proceedings of the National Academy of Sciences USA 87, 1678–1680.CrossRefGoogle ScholarPubMed