Genetic models rule out a major role of beta cell glycogen in the control of glucose homeostasis

Diabetologia

Volumn 59, Issue 5, 2016, Pages 1012-1020

  Mir Coll, Joan ^a,b   Duran, Jordi ^a,c   Slebe, Felipe ^a,c   García Rocha, Mar ^a   Gomis, Ramon ^b,c,d,e   Gasa, Rosa ^b,c   Guinovart, Joan J ^a,c,d  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e HOSPITAL CLÍNIC   (Spain)

Author keywords

Beta cell; Diabetes; Glucotoxicity; Glycogen; Glycogen synthase; Insulin secretion; Pancreatic islets

Indexed keywords

GLUCOSE; GLYCOGEN; INSULIN; MESSENGER RNA; GLYCOGEN SYNTHASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL FUNCTION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION ASSAY; GENETIC MODEL; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLYCOGEN METABOLISM; GLYCOGEN SYNTHESIS; GLYCOGENOLYSIS; HYPERINSULINEMIA; HYPOGLYCEMIA; IMMUNOBLOTTING; IN VITRO STUDY; INSULIN RELEASE; INSULIN SYNTHESIS; INSULINEMIA; LIPID DIET; MORPHOMETRICS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; WESTERN BLOTTING; ANIMAL; FEMALE; GENETICS; HOMEOSTASIS; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY;

ANIMALS; FEMALE; GLUCOSE; GLYCOGEN; GLYCOGEN SYNTHASE; HOMEOSTASIS; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; MICE, KNOCKOUT;

EID: 84955611933     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-3871-1     Document Type: Article

References (40)

1. Carpenter AM, Lazarow A (1967) Effects of hyper- and hypoglycemia on beta cell degranulation and glycogen infiltration in normal, subdiabetic and diabetic rats. Diabetes 16:493–501
2. Hellman B, Idahl LA (1969) Presence and mobilization of glycogen in mammalian pancreatic beta cells. Endocrinology 84:1–8
3. Pederson BA, Schroeder JM, Parker GE et al (2005) Glucose metabolism in mice lacking muscle glycogen synthase. Diabetes 54:3466–3473
4. Malaisse WJ, Sener A, Koser M et al (1977) The stimulus-secretion coupling of glucose-induced insulin release. Insulin release due to glycogenolysis in glucose-deprived islets. Biochem J 164:447–454
5. Weir GC, Laybutt DR, Kaneto H et al (2001) Beta cell adaptation and decompensation during the progression of diabetes. Diabetes 50:S154–S159
6. Robertson RP, Harmon J, Tran PO, Poitout V (2014) Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 53:S119–S124
7. Toreson WE (1951) Glycogen infiltration (so-called hydropic degeneration) in the pancreas in human and experimental diabetes mellitus. Am J Pathol 27:327–347
8. Malaisse WJ, Like AA, Malaisse-Lagae F et al (1968) Insulin secretion in vitro by the pancreas of the sand rat (Psammomys obesus). Diabetes 17:754–759
9. Ravelli RBG, Kalicharan RD, Avramut MC et al (2013) Destruction of tissue, cells and organelles in type 1 diabetic rats presented at macromolecular resolution. Sci Rep 3:1804
10. Graf R, Klessen C (1981) Glycogen in pancreatic islets of steroid diabetic rats. Histochemistry 73:225–232
11. Sasaki M, Arai T, Usui T, Oki Y (1991) Immunohistochemical, ultrastructural, and hormonal studies on the endocrine pancreas of voles (Microtus arvalis) with monosodium aspartate-induced diabetes. Vet Pathol 28:497–505
12. Malaisse WJ, Marynissen G, Sener A (1992) Possible role of glycogen accumulation in B cell glucotoxicity. Metabolism 41:814–819
13. Duran J, Gruart A, García-Rocha M et al (2014) Glycogen accumulation underlies neurodegeneration and autophagy impairment in Lafora disease. Hum Mol Genet 23:3147–3156
14. Duran J, Tevy MF, Garcia-Rocha M et al (2012) Deleterious effects of neuronal accumulation of glycogen in flies and mice. EMBO Mol Med 4:719–729
15. Printen JA, Brady MJ, Saltiel AR (1997) PTG, a protein phosphatase 1-binding protein with a role in glycogen metabolism. Science 275:1475–1478
16. Jurczak MJ, Danos AM, Rehrmann VR et al (2007) Transgenic overexpression of protein targeting to glycogen markedly increases adipocytic glycogen storage in mice. Am J Physiol Endocrinol Metab 292:E952–E963
17. Villarroel-Espíndola F, Maldonado R, Mancilla H et al (2013) Muscle glycogen synthase isoform is responsible for testicular glycogen synthesis: glycogen overproduction induces apoptosis in male germ cells. J Cell Biochem 114:1653–1664
18. López-Soldado I, Zafra D, Duran J et al (2015) Liver glycogen reduces food intake and attenuates obesity in a high-fat diet-fed mouse model. Diabetes 64:796–807
19. Duran J, Saez I, Gruart A et al (2013) Impairment in long-term memory formation and learning-dependent synaptic plasticity in mice lacking glycogen synthase in the brain. J Cereb Blood Flow Metab 33:550–556
20. Hingorani SR, Petricoin EF, Maitra A et al (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4:437–450
21. Altirriba J, Gasa R, Casas S et al (2010) The role of transmembrane protein 27 (TMEM27) in islet physiology and its potential use as a beta cell mass biomarker. Diabetologia 53:1406–1414
22. Fernandez-Ruiz R, Vieira E, Garcia-Roves PM, Gomis R (2014) Protein tyrosine phosphatase-1B modulates pancreatic β-cell mass. PLoS One 9:1–10
23. Cid E, Cifuentes D, Baqué S et al (2005) Determinants of the nucleocytoplasmic shuttling of muscle glycogen synthase. FEBS J 272:3197–3213
24. García-Rocha M, Roca A, de la Iglesia N et al (2001) Intracellular distribution of glycogen synthase and glycogen in primary cultured rat hepatocytes. Biochem J 357:17–24
25. Chan TM, Exton JH (1976) A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Anal Biochem 71:96–105
26. Zhu A, Romero R, Petty HR (2009) An enzymatic fluorimetric assay for glucose-6-phosphate: application in an in vitro Warburg-like effect. Anal Biochem 388:97–101
27. Nishimura M, Yokoi N, Miki T et al (2004) Construction of a multi-functional cDNA library specific for mouse pancreatic islets and its application to microarray. Mol Cell 323:315–323
28. Graf R, Tölken M (1984) Ultrastructural distribution of glycogen in pancreatic islets of steroid diabetic rats. Basic Appl Histochem 28:391–397
29. Malaisse WJ, Ladrière L, Cancelas J et al (2001) Pancreatic and hepatic glycogen content in normoglycemic and hyperglycemic rats. Mol Cell Biochem 219:45–49
30. Doherty M, Malaisse WJ (2001) Glycogen accumulation in rat pancreatic islets: in vitro experiments. Endocrine 14:303–309
31. Berman HK, O’Doherty RM, Anderson P, Newgard CB (1998) Overexpression of protein targeting to glycogen (PTG) in rat hepatocytes causes profound activation of glycogen synthesis independent of normal hormone- and substrate-mediated regulatory mechanisms. J Biol Chem 273:26421–26425
32. Malaisse WJ, Maggetto C, Leclercq-Meyer V, Sener A (1993) Interference of glycogenolysis with glycolysis in pancreatic islets from glucose-infused rats. J Clin Invest 91:432–436
33. Wicksteed B, Brissova M, Yan W et al (2010) Conditional gene targeting in mouse pancreatic beta cells. Diabetes 59:3090–3098
34. Keller C, Steensberg A, Pilegaard H et al (2001) Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J 15:2748–2750
35. Ellingsgaard H, Hauselmann I, Schuler B et al (2011) Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and alpha cells. Nat Med 17:1481–1489
36. Tuerkischer E, Wertheimer E (1942) Glycogen and adipose tissue. J Physiol 100:385–409
37. Markan KR, Jurczak MJ, Allison MB et al (2010) Enhanced glycogen metabolism in adipose tissue decreases triglyceride mobilization. Am J Physiol Endocrinol Metab 299:E117–E125
38. Saez I, Duran J, Sinadinos C et al (2014) Neurons have an active glycogen metabolism that contributes to tolerance to hypoxia. J Cereb Blood Flow Metab 34:945–955
39. Green AR, Aiston S, Greenberg CC et al (2004) The glycogenic action of protein targeting to glycogen in hepatocytes involves multiple mechanisms including phosphorylase inactivation and glycogen synthase translocation. J Biol Chem 279:46474–46482
40. Lee JY, Ristow M, Lin X et al (2006) RIP-Cre revisited, evidence for impairments of pancreatic b-cell function. J Biol Chem 281:2649–2653