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Spatial Structure of Glycogen Molecules in Cells

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Abstract

Glycogen is a strongly branched polymer of α-D-glucose, with glucose residues in the linear chains linked by 1→4-bonds (~93% of the total number of bonds) and with branching after every 4-8 residues formed by 1→6-glycosidic bonds (~7% of the total number of bonds). It is thought currently that a fully formed glycogen molecule (β-particle) with the self-glycosylating protein glycogenin in the center has a spherical shape with diameter of ~42 nm and contains ~ 55,000 glucose residues. The glycogen molecule also includes numerous proteins involved in its synthesis and degradation, as well as proteins performing a carcass function. However, the type and force of bonds connecting these proteins to the polysaccharide moiety of glycogen are significantly different. This review presents the available data on the spatial structure of the glycogen molecule and its changes under various physiological and pathological conditions.

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Abbreviations

BE:

branching enzyme

GDE:

glycogen debranching enzyme

GP:

glycogen phosphorylase

G-1-P:

glu-cose-1-phosphate

G-6-P:

glucose-6-phosphate

GPa:

active form of glycogen phosphorylase

GS:

glycogen synthase

MG:

macroglycogen

PG:

proglycogen

References

  1. Schmidt-Nielsen, K. (1982) Animal Physiology. Adaptation and Environment [Russian translation], Mir, Moscow.

    Google Scholar 

  2. Danovaro, R., Dell’Anno, A., Pusceddu, A., Gambi, C., Heiner, I., and Kristensen, R. M. (2010) The first meta-zoan living in permanently anoxic conditions, BMC Biol., 8, 30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Kasting, J. F., and Siefert, J. (2002) Life and the evolution of Earth’s atmosphere, Science, 296, 1066–1068.

    Article  PubMed  CAS  Google Scholar 

  4. Knoll, A. H. (2003) Life on a Young Planet: The First Tree Billion Years of Evolution on Earth, Princeton, Princeton University Press, Chichester.

    Google Scholar 

  5. Holand, H. D. (2006) The oxygenation of the atmosphere and oceans, Phil. Trans. R. Soc. B, 361, 903–915.

    Article  CAS  Google Scholar 

  6. Ball, S., Colleoni, C., Cenci, U., Raj, J. N., and Tirtiaux, C. (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the estab-lishment of plastid endosymbiosis, J. Exp. Botany, 62, 1775–1801.

    Article  CAS  Google Scholar 

  7. Bernard, C. (1857) Nouvelles recherches experimentales sur les phenomenes glycogeniques du foie, Mum. Soc. Biol., 4, 1–7.

    Google Scholar 

  8. Harris, R. A. (1992) Textbook of Biochemistry with Clinical Correlations (Davlin, T. M., ed.) Wiley Liss, N. Y., pp. 291–358.

    Google Scholar 

  9. Ferrer, J. C., Favre, C., Gomis, R. R., Fernandez-Novell, J. M., Garcia-Rocha, M., de la Iglesia, N., Cid, E., and Guinovart, J. J. (2003) Control of glycogen deposition, FEBS Lett., 546, 27–132.

    Article  CAS  Google Scholar 

  10. Greenberg, C. C., Jurczak, M. J., Danos, A. M., and Brady, M. J. (2006) Glycogen branches out: new perspec-tives on the role of glycogen metabolism in the integration of metabolic pathways, Am. J. Physiol. Endocrinol. Metab., 291, E1–E8.

    Google Scholar 

  11. Jurczak, M. J., Danos, A. M., Rehrmann, V. R., and Brady, M. J. (2008) The role of protein translocation in the regu-lation of metabolism, J. Cell Biochem., 104, 435–443.

    Article  PubMed  CAS  Google Scholar 

  12. Jungermann, K. (1992) Role of intralobular compartmen-tation in hepatic metabolism, Diabete Metab., 18, 81–86.

    PubMed  CAS  Google Scholar 

  13. Rajvanshi, P., Liu, D., Ott, M., Gagandeep, S., Schilsky, M. L., and Gupta, S. (1998) Fractionation of rat hepato-cyte subpopulations with varying metabolic potential, pro-liferative capacity, and retroviral gene transfer efficiency, Exp. Cell. Res., 244, 405–419.

    Article  PubMed  CAS  Google Scholar 

  14. Teutsch, H. F., Schuerfeld, D., and Groezinger, E. (1999) Three-dimensional reconstruction of parenchymal units in the liver of the rat, Hepatology, 29, 494–505.

    Article  PubMed  CAS  Google Scholar 

  15. Kudryavtseva, M. V., Bezborodkina, N. N., Radchenko, V. G., Okovity, S. V., and Kydryavtsev, B. N. (2001) Metabolic heterogeneity of glycogen in hepatocytes of patients with liver cirrhosis: the glycogen of the liver lobule zones in cir-rhosis, Europ. J. Gastroenterol. Hepatol., 13, 693–697.

    Article  CAS  Google Scholar 

  16. Roach, P. J., Depaoli-Roach, A. A., Hurley, T. D., and Tagliabracci, V. S. (2012) Glycogen and its metabolism: some new development and old themes, Biochem. J., 441, 763–787.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Shearer, J., and Graham, T. E. (2004) Novel aspects of skeletal muscle glycogen and its regulation during rest and exercise, Exerc. Sport. Sci. Rev., 32, 120–126.

    Article  PubMed  Google Scholar 

  18. Roach, P. J. (2002) Glycogen and its metabolism, Curr. Mol. Med., 2, 101–120.

    Article  PubMed  CAS  Google Scholar 

  19. Minassian, B. A., Lee, J. R., Herbrick, J. A., Huizenga, J., Soder, S., Mungall, A. J., Dunham, I., Gardner, R., Fong, C. Y., Carpenter, S., Jardim, L., Satishchandra, P., Andermann, E., Snead, O. C., 3rd, Lopes-Cendes, I., Tsui, L. C., Delgado-Escueta, A. V., Rouleau, G. A., and Scherer, S. W. (1998) Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy, Nat. Genet., 20, 171–174.

    Article  PubMed  CAS  Google Scholar 

  20. Ganesh, S., Amano, K., Delgado-Escueta, A. V., and Yamakawa, K. (1999) Isolation and characterization of mouse homologue for the human epilepsy gene, Biochem. Biophys. Res. Commun., 257, 24–28.

    Article  PubMed  CAS  Google Scholar 

  21. Jiang, S., Heller, B., Tagliabracci, V. S., Zhai, L., Irimia, J. M., Depaoli-Roach, A. A., Wells, C. D., Skurat, A. V., and Roach, P. J. (2010) Starch binding domain-containing pro-tein 1/genethonin 1 is a novel participant in glycogen metabolism, J. Biol. Chem., 285, 34960–34971.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Stapleton, D., Nelson, C., Parsawar, K., McClain, D., Gilbert-Wilson, R., Barker, E., Rudd, B., Brown, K., Hendrix, W., O’Donnell, P., and Parker, G. (2010) Analysis of hepatic glycogen-associated proteins, Proteomics, 10, 2320–2329.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Caudwell, F. B., and Cohen, P. (1980) Purification and subunit structure of glycogen-branching enzyme from rab-bit skeletal muscle, Eur. J. Biochem., 109, 391–394.

    Article  PubMed  CAS  Google Scholar 

  24. Krisman, C. R., and Barengo, R. A. (1975) A precursor of glycogen biosynthesis: alpha-1,4-glucan-protein, Eur. J. Biochem., 52, 117–123.

    Article  PubMed  CAS  Google Scholar 

  25. Alonso, M. D., Lomako, J., Lomako, W. M., and Whelan, W. J. (1995) A new look at the biogenesis of glycogen, FASEB J., 9, 1126–1137.

    Article  PubMed  CAS  Google Scholar 

  26. Cao, Y., Mahrenholz, A. M., DePaoli-Roach, A. A., and Roach, P. J. (1993) Characterization of rabbit skeletal mus-cle glycogenin: tyrosine 194 is essential for function, J. Biol. Chem., 268, 14687–14693.

    PubMed  CAS  Google Scholar 

  27. Hurley, T. D., Walls, C., Bennett, J. R., Roach, P. J., and Wang, M. (2006) Direct detection of glycogenin reaction products during glycogen initiation, Biochem. Biophys. Res. Commun., 348, 374–378.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Roach, P. J., and Skurat, A. V. (1997) Self-glucosylating initiator proteins and their role in glycogen biosynthesis, Prog. Nucleic Acid Res. Mol. Biol., 57, 289–316.

    Article  PubMed  CAS  Google Scholar 

  29. Lomako, J., Lomako, W. M., and Whelan, W. J. (2004) Glycogenin: the primer for mammalian and yeast glycogen synthesis, Biochim. Biophys. Acta, 1673, 45–55.

    Article  PubMed  CAS  Google Scholar 

  30. Fernandez-Novell, J. M., Lopez-Iglesias, C., Ferrer, J. C., and Guinovart, J. J. (2002) Zonal distribution of glycogen syn-thesis in isolated rat hepatocytes, FEBS Lett., 531, 222–228.

    Article  PubMed  CAS  Google Scholar 

  31. Larner, J. (1955) Branching enzyme from liver, Methods Enzymol., 1, 222–225.

    Article  CAS  Google Scholar 

  32. Krisman, C. R. (1962) α-l,4-Glucan: α-l,4-glucan 6-glyco-syltransferase from liver, Biochim. Biophys. Acta, 65, 307–315.

    Article  CAS  Google Scholar 

  33. Brown, B. I., and Brown, D. H. (1966) α-l,4-Glucan 6-glycosyltransferase from mammalian muscle, Methods Enzymol., 8, 395–403.

    Article  CAS  Google Scholar 

  34. Melendez, R., Melendez-Hevia, E., and Cascante, M. (1997) How did glycogen structure evolve to satisfy the requirement for rapid mobilization of glucose? A problem of physical constraints in structure building, J. Mol. Evol., 45, 446–455.

    Article  PubMed  CAS  Google Scholar 

  35. Bezborodkina, N. N., Okovityi, S. V., and Kudryavtsev, B. N. (2008) Carbohydrate Metabolism in Chronic Damages of the Liver [in Russian], Sintez-Buk, St. Petersburg.

    Google Scholar 

  36. Biorn, A. C., and Graves, D. J. (2001) The amino-terminal tail of glycogen phosphorylase is a switch for controlling phosphorylase conformation, activation, and response to ligands, Biochemistry, 40, 5181–5189.

    Article  PubMed  CAS  Google Scholar 

  37. Newsholm, E., and Start, C. (1977) Regulation in Metabolism [Russian translation], Mir, Moscow.

    Google Scholar 

  38. Goldsmith, E., Sprang, S., and Fletterick, R. (1982) Structure of maltoheptaose by difference Fourier methods and a model for glycogen, J. Mol. Biol., 156, 411–427.

    Article  PubMed  CAS  Google Scholar 

  39. Geddes, R., Jeyarathan, P., and Taylor, J. A. (1992) Molecular and metabolic aspects of lysosomal glycogen, Carbohydr. Res., 227, 339–349.

    Article  PubMed  CAS  Google Scholar 

  40. Geddes, R. (1985) The Polysaccharides, Vol. 3 (Aspinall, G. O., ed.), Academic Press, Orlando, pp. 283–336.

  41. Stepanenko, B. N., and Bobrova, L. N. (1974) Modern concepts about micro-and macromolecular structure of glycogen, Usp. Biol. Khim., 15, 195–207.

    CAS  Google Scholar 

  42. Geddes, R., and Stratton, G. C. (1977) The influence of lysosomes on glycogen metabolism, Biochem. J., 163, 193–200.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Wanson, J. C., and Drochmans, P. (1968) Rabbit skeletal muscle glycogen. A morphological and biochemical study of glycogen β-particles isolated by the precipitation-cen-trifugation method, J. Cell Biol., 38, 130–150.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Devos, P., Baudhuin, P., Van Hoof, F., and Hers, H. G. (1983) The alpha particulate liver glycogen. A morphomet-ric approach to the kinetics of its synthesis and degradation, Biochem. J., 209, 159–165.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Rybicka, K. K. (1996) Glycosomes–the organelles of glycogen metabolism, Tissue Cell, 28, 253–265.

    Article  PubMed  CAS  Google Scholar 

  46. Sullivan, M. A., Vilaplana, F., Cave, R. A., Stapleton, D., Gray-Weale, A. A., and Gilbert, R. G. (2010) Nature of α-and β-particles in glycogen using molecular size distribu-tions, Biomacromolecules, 11, 1094–1100.

    Article  PubMed  CAS  Google Scholar 

  47. Besford, Q. A., Sullivan, M. A., Zheng, L., Gilbert, R. G., Stapleton, D., and Gray Weale, A. (2012) The structure of cardiac glycogen in healthy mice, Int. J. Biol. Macromol., 51, 887–891.

    Article  PubMed  CAS  Google Scholar 

  48. Devos, P., and Hers, H. G. (1979) A molecular order in the synthesis and degradation of glycogen in the liver, Eur. J. Biochem., 99, 161–167.

    Article  PubMed  CAS  Google Scholar 

  49. Devos, P., and Hers, H. G. (1980) Glycogen in rat adipose tissue: sequential synthesis and random degradation, Biochem. Biophys. Res. Commun., 95, 1031–1036.

    Article  PubMed  CAS  Google Scholar 

  50. Orrell, S. A., and Bueding, E. (1964) A comparison of products obtained by various procedures used for the extraction of glycogen, J. Biol. Chem., 239, 4021–4026.

    PubMed  CAS  Google Scholar 

  51. Nakamura, M. (1977) Handbook of Starch Science, Asakura-Shoten, Tokyo.

    Google Scholar 

  52. Hata, K., Hata, M., Hata, M., and Matsuda, K. (1984) A proposed model of glycogen particle, J. Jpn. Soc. Starch. Sci., 31, 146–155.

    Article  CAS  Google Scholar 

  53. Sullivan, M. A., Aroney, S. T., Li, S., Warren, F. J., Joo, J. S., Mak, K. S., Stapleton, D. I., Bell-Anderson, K. S., and Gilbert, R. G. (2014) Molecular insights into glycogen α-particle formation, Biomacromolecules, 15, 660–665.

    Article  PubMed  CAS  Google Scholar 

  54. Stetten, M. R., and Stetten, D., Jr. (1958) Influence of molecular size of glycogen on the phosphorylase reaction, J. Biol. Chem., 232, 489–504.

    PubMed  CAS  Google Scholar 

  55. Melendez-Hevia, E., Waddell, T. G., and Shelton, E. D. (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule, Biochem. J., 295 (Pt. 2), 477–483.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Meyer, R. H., and Bernfeld, P. (1940) Recherches sur l’amidon V. L’amilopectine, Helv. Chim. Acta, 23, 875–885.

    Article  CAS  Google Scholar 

  57. Whelan, W. J. (1971) Enzymic explorations of the struc-tures of starch and glycogen, Biochem. J., 122, 609–622.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Walker, G. J., and Whelan, W. J. (1960) The mechanism of carbohydrase action. 8. Structures of the muscle-phospho-rylase limit dextrins of glycogen and amylopectin, Biochem. J., 76, 264–270.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Shearer, J., and Graham, T. E. (2002) New perspectives on the storage and organization of muscle glycogen, J. Appl. Physiol., 27, 179–203.

    Article  CAS  Google Scholar 

  60. Graham, T. E., Yuan, Z., Hill, A. K., and Wilson, R. J. (2010) The regulation of muscle glycogen: the granule and its proteins, Acta Physiol., 199, 489–498.

    Article  CAS  Google Scholar 

  61. Madsen, N. B., and Cori, C. F. (1958) The binding of glycogen and phosphorylase, J. Biol. Chem., 233, 1251–1256.

    PubMed  CAS  Google Scholar 

  62. Melendez, R., Melendez-Hevia, E., Mas, F., Mach, J., and Cascante, M. (1998) The fractal structure of glycogen: a clever solution to optimize cell metabolism, Biophys. J., 75, 106–114.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Melendez-Hevia, E., Waddel, T. G., Raposo, R. R., and Lupianez, J. A. (1995) Evolution of metabolism: optimiza-tion of glycogen structure, J. Biol. Systems, 3, 177–186.

    Article  Google Scholar 

  64. Geddes, R. (1986) Glycogen: a metabolic viewpoint, Bioscience Rep., 6, 415–428.

    Article  CAS  Google Scholar 

  65. Marshall, J. J. (1974) Application of enzymic methods to the structural analysis of polysaccharides, Adv. Carbohydr. Chem. Biochem., 30, 257–370.

    Article  PubMed  CAS  Google Scholar 

  66. Gunja-Smith, Z., Marshall, J. J., Mercier, C., Smith, E. E., and Whelan, W. J. (1970) A revision of the Meyer–Bernfeld model of glycogen and amylopectin, FEBS Lett., 12, 101–104.

    Article  PubMed  CAS  Google Scholar 

  67. Gessler, K., Uson, I., Takaha, T., Krauss, N., Smith, S. M., Okada, S., Sheldrick, G. M., and Saenger, W. (1999) V-amylose at atomic resolution: X-ray structure of a cycloamylose with 26 glucose residues (cyclomaltohexa-icosaose), Proc. Natl. Acad. Sci. USA, 96, 4246–4251.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Mercier, C., and Whelan, W. J. (1970) The fine structure of glycogen from type IV glycogen storage disease, Eur. J. Biochem., 16, 579–583.

    Article  PubMed  CAS  Google Scholar 

  69. Garyaly, P., Segvich, D. M., DePaoli-Roach, A. A., and Roach, P. J. (2014) Protein degradation and quality control in cells from laforin and malin knockout mice, J. Biol. Chem., 289, 20606–20614.

    Article  CAS  Google Scholar 

  70. Jiang, S., Wells, C. D., and Roach, P. J. (2011) Starch-binding domain-containing protein 1 (Stbd1) and glycogen metabolism: identification of the Atg8 family interacting motif (AIM) in Stbd1 required for interaction with GABARAPL1, Biochem. Biophys. Res. Commun., 413, 420–425.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Sun, T., Yi, H., Yang, C., Kishnani, P. S., and Sun, B. (2016) Starch binding domain-containing protein 1 plays a dominant role in glycogen transport to lysosomes in liver, J. Biol. Chem., 291, 16479–16484.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Willstatter, R., and Rhodewald, M. (1934) Protein binding of physiologically important substances. The conditions of glycogen in liver, muscle and leucocytes, Z. Physiol. Chem., 225, 103–124.

    Article  CAS  Google Scholar 

  73. Bloom, W. L., Lewis, G. T., Schumpert, M. Z., and Tsung-men Shen (1951) Glycogen fractions of liver and muscle, J. Biol. Chem., 188, 631–636.

    PubMed  CAS  Google Scholar 

  74. Russel, J. A., and Bloom, W. L. (1955) Extractable and residual glycogen in tissues of the rat, Am. J. Physiol., 183, 345–355.

    Google Scholar 

  75. Weisberg, J., and Rodbard, S. (1958) Distribution of glyco-gen in the rat heart, Am. J. Physiol., 193, 466–468.

    PubMed  CAS  Google Scholar 

  76. Kugler, J. H., and Wilkinson, W. J. (1959) A relation between total glycogen content of ox myocardium and its histochemical demonstration, J. Histochem. Cytochem., 7, 298–402.

    Article  Google Scholar 

  77. Kugler, J. H., and Wilkinson, W. J. (1960) Glycogen frac-tions and their role in the histochemical detection of glyco-gen, J. Histochem. Cytochem., 8, 195–199.

    Article  PubMed  CAS  Google Scholar 

  78. Kugler, J. H., and Wilkinson, W. J. (1961) The basis for the histochemical detection of glycogen, J. Histochem. Cytochem., 9, 498–503.

    Article  PubMed  CAS  Google Scholar 

  79. Kudryavtseva, M. V., Kudryavtsev, B. N., and Rozanov, Y. M. (1974) About two fractions of glycogen in the cells of rat liver (cytofluorimetric study), Tsitologiya, 16, 851–858.

    CAS  Google Scholar 

  80. Prins, D. A., and Jeanlos, R. W. (1948) Chemistry of the carbohydrates, Annu. Rev. Biochem., 17, 67–96.

    Article  PubMed  CAS  Google Scholar 

  81. Kits Van Heijningen, A. J., and Kemp, A. (1955) Free and fixed glycogen in rat muscle, Biochem. J., 59, 487–491.

    Article  Google Scholar 

  82. Rozenfeld, E. L., and Popova, I. A. (1979) Glycogen Disease [in Russian], Meditsina, Moscow.

    Google Scholar 

  83. Lomako, J., Lomako, W. M., and Whelan, W. J. (1991) Proglycogen: a low-molecular-weight of muscle glycogen, FEBS Lett., 279, 223–228.

    Article  PubMed  CAS  Google Scholar 

  84. Lomako, J., Lomako, W. M., Whelan, W. J., Dombro, R. S., Neary, J. T., and Norenberg, M. D. (1993) Glycogen synthesis in the astrocyte: from glycogenin to proglycogen to glycogen, FASEB J., 7, 1386–1393.

    Article  PubMed  CAS  Google Scholar 

  85. Shearer, J., Graham, T. E., Battram, D. S., Robinson, D. L., Richter, E. A., Wilson, R. J., and Bakovic, M. (2005) Glycogenin activity and mRNA expression in response to volitional exhaustion in human skeletal muscle, J. Appl. Physiol., 99, 957–962.

    Article  PubMed  CAS  Google Scholar 

  86. Kraniou, Y., Cameron-Smith, D., Misso, M., Collier, G., and Hargreaves, M. (2000) Effects of exercise on GLUT-4 and glycogenin gene expression in human skeletal muscle, J. Appl. Physiol., 88, 794–796.

    Article  PubMed  CAS  Google Scholar 

  87. Arkinstall, M. J., Bruce, C. R., Clark, S. A., Rickards, C. A., Burke, L. M., and Hawley, J. A. (2004) Regulation of fuel metabolism by pre-exercise muscle glycogen content and exercise intensity, J. Appl. Physiol., 97, 2275–2283.

    Article  PubMed  CAS  Google Scholar 

  88. Marchand, I., Tarnopolsky, M., Adamo, K. B., Bourgeois, J. M., Chorneyko, K., and Graham, T. E. (2007) Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise, J. Physiol., 580 (Pt. 2), 617–628.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Adamo, K. B., and Graham, T. E. (1998) Comparison of traditional measurement with macroglycogen and pro-glycogen analysis of muscle glycogen, J. Appl. Physiol., 84, 908–913.

    Article  PubMed  CAS  Google Scholar 

  90. Battram, D. S., Shearer, J., Robinson, D., and Graham, T. E. (2004) Caffeine ingestion does not impede the resyn-thesis of proglycogen and macroglycogen after prolonged exercise and carbohydrate supplementation in humans, J. Appl. Physiol., 96, 943–950.

    Article  PubMed  CAS  Google Scholar 

  91. Wilson, R. J. (2009) Relating Glycogenin Protein Levels and Glycogen Content Post-contraction in Human and Rodent Skeletal Muscle, Thesis University Guelph.

    Google Scholar 

  92. Granlund, A., Jensen-Waern, M., and Essen-Gustavsson, B. (2011) The influence of the PRKAG3 mutation on glycogen, enzyme activities and fibre types in different skeletal muscles of exercise trained pigs, Acta Vet. Scand., 53, 20.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Graham, T. E., Adamo, K. B., Shearer, J., Marchand, I., and Saltin, B. (2001) Pro-and macroglycogenolysis: rela-tionship with exercise intensity and duration, J. Appl. Physiol., 90, 873–879.

    Article  PubMed  CAS  Google Scholar 

  94. James, A. P., Barnes, P. D., Palmer, T. N., and Fournier, P. A. (2008) Proglycogen and macroglycogen: artifacts of glycogen extraction? Metabolism, 57, 535–543.

    Article  PubMed  CAS  Google Scholar 

  95. Kudryavtseva, M. V., and Shalakhmetova, T. M. (1976) Microfluorimetrical study of glycogen fractions in the cells of rat liver under different conditions of liver perfusion and animal nutrition, Tsitologiya, 18, 506–509.

    CAS  Google Scholar 

  96. Kudryavtseva, M. V., Skorina, A. D., and Kudryavtsev, B. N. (1988) Cytofluorimetrical study of glycogen fractions in cells of the liver from patients with chronic viral and alco-hol hepatitis, Tsitologiya, 30, 705–709.

    Google Scholar 

  97. Kudryavtseva, M. V., Emel’yanov, A. V., Sakuta, G. A., Skorina, A. D., Sleptsova, L. A., and Kudryavtsev, B. N. (1992) Cytofluorimetrical study of glycogen content and its fractions in hepatocytes of patients with liver cirrhosis of different etiology, Tsitologiya, 34, 100–107.

    Google Scholar 

  98. Kudryavtseva, M. V., Bezborodkina, N. N., Radchenko, V. G., Okovity, S. V., Ivanova, O. V., and Kudryavtsev, B. N. (2000) Metabolic heterogeneity of glycogen in hepato-cytes of patients with liver cirrhosis, Tsitologiya, 42, 550–554.

    CAS  Google Scholar 

  99. Kudryavtseva, M. V., Bezborodkina, N. N., Okovity, S. V., and Kudryavtsev, B. N. (2002) Study on the influence of bemithyl on the carbohydrate metabolism of the cirrhoti-cally-altered rat liver, Tsitologiya, 44, 166–174.

    CAS  Google Scholar 

  100. Kudryavtseva, M. V., Bezborodkina, N. N., Okovity, S. V., and Kudryavtsev, B. N. (2003) Effects of the 2-ethyl-thiobenzimidazole hydrobromide (bemithyl) on carbohy-drate metabolism in cirrhotic rat liver, Exp. Toxic. Pathol., 54, 339–347.

    Article  CAS  Google Scholar 

  101. Kudryavtseva, M. V., and Shalakhmetova, T. M. (1979) Cytofluorimetric study of glycogen contents and its frac-tions in the cells of rat liver during the 1st week of post-natal ontogenesis, Tsitologiya, 21, 566–571.

    CAS  Google Scholar 

  102. Kudryavtseva, M. V., and Zavadskaya, E. E. (1982) Cytofluorimetric study of glycogen contents and its frac-tions in the cells of rat liver under conditions of its synthe-sis and degradation, Tsitologiya, 24, 777–783.

    CAS  Google Scholar 

  103. Kudryavtseva, M. V., Sakuta, G. A., Stein, G. I., and Kudryavtsev, B. N. (1990) Dynamics of glycogen synthesis in hepatocytes from different lobes of the rat liver, Tsitologiya, 32, 1010–1018.

    CAS  Google Scholar 

  104. Kudryavtseva, M. V., Emel’yanov, A. V., Sakuta, G. A., Bezborodkina, N. N., and Kudryavtsev, B. N. (1998) Rehabilitation of the glycogen-generating function of hepatocytes of the cirrhotic rat liver on the high-carbohy-drate diet, Tsitologiya, 40, 133–142.

    CAS  Google Scholar 

  105. Chestnova, A. Y. (2016) The Content and Structure of Glycogen in Hepatocytes of Human and Rat Normal and Cirrhotic Liver, Candidates’ dissertation (in Biology) [in Russian], Institute of Cytology, Russian Academy of Sciences, St. Petersburg.

    Google Scholar 

  106. Ghosh, P., Heath, A. C., Donahue, M. J., and Masaracchia, R. A. (1989) Glycogen synthesis in the obliquely striated muscle of Ascaris suum, Eur. J. Biochem., 183, 679–685.

    Article  PubMed  CAS  Google Scholar 

  107. Farkas, I., Hardy, T. A., Goebl, M. G., and Roach, P. J. (1991) Two glycogen synthase isoforms in Saccharomyces cerevisiae are coded by distinct genes that are differential-ly controlled, J. Biol. Chem., 266, 15602–15607.

    PubMed  CAS  Google Scholar 

  108. Sjostrom, M., Friden, J., and Ekblom, B. (1982) Fine structural details of human muscle fibres after fibre type specific glycogen depletion, Histochemistry, 76, 425–438.

    Article  PubMed  CAS  Google Scholar 

  109. Elsner, P., Quistorff, B., Hansen, G. H., and Grunnet, N. (2002) Partly ordered synthesis and degradation of glyco-gen in cultured rat myotubes, J. Biol. Chem., 277, 4831–4838.

    Article  PubMed  CAS  Google Scholar 

  110. Van der Kleji, B. J. (1951) A rapid determination of glyco-gen in tissues, Biochim. Biophys. Acta, 7, 481–482.

    Article  Google Scholar 

  111. Powell, P. O., Sullivan, M. A., Sheehy, J. J., Schulz, B. L., Warren, F. J., and Gilbert, R. G. (2015) Acid hydrolysis and molecular density of phytoglycogen and liver glycogen helps understand the bonding in glycogen α (composite) particles, PloS One, 10, e0134065.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Stetten, M. R., and Stetten, D., Jr. (1954) A study of the nature of glycogen regeneration in the intact animal, J. Biol. Chem., 207, 331–340.

    PubMed  CAS  Google Scholar 

  113. Roach, P. J., Skurat, A. V., and Harris, R. A. (2001) Handbook of Physiology. Section 7: The Endocrine System. Vol. II. The Endocrine Pancreas and Regulation of Metabolism (Jefferson, L. S., and Cherrington, A. D., eds.), Oxford University Press, Oxford, pp. 609–647.

    Google Scholar 

  114. Prats, C., Helge, J. W., Nordby, P., Qvortrup, K., Ploug, T., Dela, F., and Wojtaszewski, J. F. (2009) Dual regulation of muscle glycogen synthase during exercise by activation and compartmentalization, J. Biol. Chem., 284, 15692–15700.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. DiNuzzo, M. (2013) Kinetic analysis of glycogen turnover: relevance to human brain 13C-NMR spectroscopy, J. Cereb. Blood Flow Metab., 33, 1540–1548.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Fessenden, J. D. (2009) Forster resonance energy transfer measurements of ryanodine receptor type 1 structure using a novel site-specific labeling method, PloS One, 4, e7338.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Grecco, H. E., and Verveer, P. J. (2011) FRET in cell biol-ogy: still shining in the age of super-resolution? ChemPhysChem, 12, 484–490.

    Article  PubMed  CAS  Google Scholar 

  118. Miyawaki, A. (2011) Development of probes for cellular functions using fluorescent proteins and fluorescence res-onance energy transfer, Annu. Rev. Biochem., 80, 357–373.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Cytology, Russian Academy of Sciences, 194064, St. Petersburg, Russia

    N. N. Bezborodkina, A. Yu. Chestnova, M. L. Vorobev & B. N. Kudryavtsev

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  1. N. N. Bezborodkina
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  2. A. Yu. Chestnova
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  3. M. L. Vorobev
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  4. B. N. Kudryavtsev
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Correspondence to N. N. Bezborodkina.

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Original Russian Text © N. N. Bezborodkina, A. Yu. Chestnova, M. L. Vorobev, B. N. Kudryavtsev, 2018, published in Biokhimiya, 2018, Vol. 83, No. 5, pp. 627–644.

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Bezborodkina, N.N., Chestnova, A.Y., Vorobev, M.L. et al. Spatial Structure of Glycogen Molecules in Cells. Biochemistry Moscow 83, 467–482 (2018). https://doi.org/10.1134/S0006297918050012

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  • DOI: https://doi.org/10.1134/S0006297918050012

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