Polyglucosan neurotoxicity caused by glycogen branching enzyme deficiency can be reversed by inhibition of glycogen synthase

Journal of Neurochemistry

Volumn 127, Issue 1, 2013, Pages 101-113

  Kakhlon, Or ^a   Glickstein, Hava ^b   Feinstein, Naomi ^c   Liu, Yan ^d   Baba, Otto ^e   Terashima, Tatsuo ^f   Akman, Hasan Orhan ^g   Dimauro, Salvatore ^g   Lossos, Alexander ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d Center for Cancer and Immunology Research Children's National Medical Center   (United States)

^e OHU UNIVERSITY   (Japan)

^f TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^g Department of Medicine   (United States)

Author keywords

adult polyglucosan body disease; autophagy; glycogen branching enzyme; glycogen synthase; polyglucosan; polyglucosan bodies

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; CARBOHYDRATE DERIVATIVE; GLYCOGEN SYNTHASE; POLYGLUCOSAN; RAPAMYCIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VINBLASTINE;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; BINDING SITE; BRAIN NERVE CELL; CELL PROTECTION; CONTROLLED STUDY; DEPHOSPHORYLATION; DRUG MECHANISM; EMBRYO; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; FEMALE; GLYCOGEN STORAGE DISEASE; HUMAN; HUMAN CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STARVATION;

ADULT POLYGLUCOSAN BODY DISEASE; AUTOPHAGY; GLYCOGEN BRANCHING ENZYME; GLYCOGEN SYNTHASE; POLYGLUCOSAN; POLYGLUCOSAN BODIES;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; ADENOSINE TRIPHOSPHATE; AGED; ANIMALS; APOPTOSIS; CEREBRAL CORTEX; ENZYME INHIBITORS; FEMALE; FIBROBLASTS; GLUCANS; GLYCOGEN STORAGE DISEASE; GLYCOGEN SYNTHASE; HUMANS; LYMPHOCYTES; MICROSCOPY, FLUORESCENCE; NEUROTOXICITY SYNDROMES; PHOSPHORYLATION; PRIMARY CELL CULTURE; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; STARVATION; TOR SERINE-THREONINE KINASES; TRANSDUCTION, GENETIC;

EID: 84884902969     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12277     Document Type: Article

References (43)

1. Aguado C., Sarkar S., Korolchuk V. I., Criado O., Vernia S., Boya P., Sanz P., de Cordoba S. R., Knecht E., and, Rubinsztein D. C., (2010) Laforin, the most common protein mutated in Lafora disease, regulates autophagy. Hum. Mol. Genet. 19, 2867-2876.
2. Akman H. O., Sheiko T., Tay S. K., Finegold M. J., Dimauro S., and, Craigen W. J., (2011) Generation of a novel mouse model that recapitulates early and adult onset glycogenosis type IV. Hum. Mol. Genet. 20, 4430-4439.
3. Andrade D. M., Turnbull J., and, Minassian B. A., (2007) Lafora disease, seizures and sugars. Acta Myol. 26, 83-86.
4. Ashe K. M., Taylor K. M., Chu Q., et al,. (2010) Inhibition of glycogen biosynthesis via mTORC1 suppression as an adjunct therapy for Pompe disease. Mol. Genet. Metab. 100, 309-315.
5. Assereto S., van Diggelen O. P., Diogo L., et al,. (2007) Null mutations and lethal congenital form of glycogen storage disease type IV. Biochem. Biophys. Res. Commun. 361, 445-450.
6. Baskaran S., Chikwana V. M., Contreras C. J., Davis K. D., Wilson W. A., DePaoli-Roach A. A., Roach P. J., and, Hurley T. D., (2011) Multiple glycogen-binding sites in eukaryotic glycogen synthase are required for high catalytic efficiency toward glycogen. J. Biol. Chem. 286, 33999-34006.
7. Belanger M., Allaman I., and, Magistretti P. J., (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724-738.
8. Benarroch E. E., (2010) Glycogen metabolism: metabolic coupling between astrocytes and neurons. Neurology 74, 919-923.
9. Boland B., Kumar A., Lee S., Platt F. M., Wegiel J., Yu W. H., and, Nixon R. A., (2008) Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 28, 6926-6937.
10. Bouskila M., Hunter R. W., Ibrahim A. F., Delattre L., Peggie M., van Diepen J. A., Voshol P. J., Jensen J., and, Sakamoto K., (2010) Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab. 12, 456-466.
11. Bultot L., Guigas B., Von Wilamowitz-Moellendorff A., et al,. (2012) AMP-activated protein kinase phosphorylates and inactivates liver glycogen synthase. Biochem. J. 443, 193-203.
12. Calvetti D., and, Somersalo E., (2012) Menage a trois: the role of neurotransmitters in the energy metabolism of astrocytes, glutamatergic, and GABAergic neurons. J. Cereb. Blood Flow Metab. 32, 1472-1483.
13. Cavanagh J. B., (1999) Corpora-amylacea and the family of polyglucosan diseases. Brain Res. Brain Res. Rev. 29, 265-295.
14. Chan E. M., Ackerley C. A., Lohi H., Ianzano L., Cortez M. A., Shannon P., Scherer S. W., and, Minassian B. A., (2004) Laforin preferentially binds the neurotoxic starch-like polyglucosans, which form in its absence in progressive myoclonus epilepsy. Hum. Mol. Genet. 13, 1117-1129.
15. Chander B. S., and, Chakravarthy V. S., (2012) A computational model of neuro-glio-vascular loop interactions. PLoS ONE 7, e48802.
16. Chen Y., and, Bucherell A,. (1995) Glycogen storage diseases, in The Metabolic and Molecular Bases of Inherited Diseases (, Scriver C. R., Beaudet A. L., Sly W. S., and, Valle D., eds), 7th edn, pp 935-965. McGraw-Hill, New York.
17. Choi H. B., Gordon G. R., Zhou N., et al,. (2012) Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 75, 1094-1104.
18. Das G. C., and, Hollinger F. B., (2012) Molecular pathways for glucose homeostasis, insulin signaling and autophagy in hepatitis C virus induced insulin resistance in a cellular model. Virology 434, 5-17.
19. DiNuzzo M., Mangia S., Maraviglia B., and, Giove F., (2010) Glycogenolysis in astrocytes supports blood-borne glucose channeling not glycogen-derived lactate shuttling to neurons: evidence from mathematical modeling. J. Cereb. Blood Flow Metab. 30, 1895-1904.
20. Douillard-Guilloux G., Raben N., Takikita S., et al,. (2010) Restoration of muscle functionality by genetic suppression of glycogen synthesis in a murine model of Pompe disease. Hum. Mol. Genet. 19, 684-696.
21. Hayashi-Nishino M., Fujita N., Noda T., Yamaguchi A., Yoshimori T., and, Yamamoto A., (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437.
22. Heni M., Hennige A. M., Peter A., Siegel-Axel D., Ordelheide A. M., Krebs N., Machicao F., Fritsche A., Haring H. U., and, Staiger H., (2011) Insulin promotes glycogen storage and cell proliferation in primary human astrocytes. PLoS ONE 6, e21594.
23. Kochl R., Hu X. W., Chan E. Y., and, Tooze S. A., (2006) Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 7, 129-145.
24. Kollberg G., Tulinius M., Gilljam T., Ostman-Smith I., Forsander G., Jotorp P., Oldfors A., and, Holme E., (2007) Cardiomyopathy and exercise intolerance in muscle glycogen storage disease 0. N. Engl. J. Med. 357, 1507-1514.
25. Kotoulas O. B., Kalamidas S. A., and, Kondomerkos D. J., (2004) Glycogen autophagy. Microsc. Res. Tech. 64, 10-20.
26. Lamperti C., Salani S., Lucchiari S., et al,. (2009) Neuropathological study of skeletal muscle, heart, liver, and brain in a neonatal form of glycogen storage disease type IV associated with a new mutation in GBE1 gene. J. Inherit. Metab. Dis. 32 (Suppl 1), S161-S168.
27. Lee J. W., Park S., Takahashi Y., and, Wang H. G., (2010) The association of AMPK with ULK1 regulates autophagy. PLoS ONE 5, e15394.
28. Lossos A., Barash V., Soffer D., Argov Z., Gomori M., Ben-Nariah Z., Abramsky O., and, Steiner I., (1991) Hereditary branching enzyme dysfunction in adult polyglucosan body disease: a possible metabolic cause in two patients. Ann. Neurol. 30, 655-662.
29. Magistretti P. J., and, Allaman I., (2007) Glycogen: a Trojan horse for neurons. Nat. Neurosci. 10, 1341-1342.
30. Magoulas P. L., El-Hattab A. W., Roy A., Bali D. S., Finegold M. J., and, Craigen W. J., (2012) Diffuse reticuloendothelial system involvement in type IV glycogen storage disease with a novel GBE1 mutation: a case report and review. Hum. Pathol. 43, 943-951.
31. Nakamura-Tsuruta S., Yasuda M., Nakamura T., Shinoda E., Furuyashiki T., Kakutani R., Takata H., Kato Y., and, Ashida H., (2012) Comparative analysis of carbohydrate-binding specificities of two anti-glycogen monoclonal antibodies using ELISA and surface plasmon resonance. Carbohydr. Res. 350, 49-54.
32. Pederson B. A., Schroeder J. M., Parker G. E., Smith M. W., DePaoli-Roach A. A., and, Roach P. J., (2005) Glucose metabolism in mice lacking muscle glycogen synthase. Diabetes 54, 3466-3473.
33. Schiaffino S., Mammucari C., and, Sandri M., (2008) The role of autophagy in neonatal tissues: just a response to amino acid starvation? Autophagy 4, 727-730.
34. Skurat A. V., and, Roach P. J., (1995) Phosphorylation of sites 3a and 3b (Ser640 and Ser644) in the control of rabbit muscle glycogen synthase. J. Biol. Chem. 270, 12491-12497.
35. Striano P., Zara F., Turnbull J., Girard J. M., Ackerley C. A., Cervasio M., De Rosa G., Del Basso-De Caro M. L., Striano S., and, Minassian B. A., (2008) Typical progression of myoclonic epilepsy of the Lafora type: a case report. Nat. Clin. Pract. Neurol. 4, 106-111.
36. Tiberia E., Turnbull J., Wang T., et al,. (2012) Increased laforin and laforin binding to glycogen underlie Lafora body formation in malin-deficient Lafora disease. J. Biol. Chem. 287, 25650-25659.
37. Turnbull J., Wang P., Girard J. M., et al,. (2010) Glycogen hyperphosphorylation underlies lafora body formation. Ann. Neurol. 68, 925-933.
38. Turnbull J., DePaoli-Roach A. A., Zhao X., et al,. (2011) PTG depletion removes Lafora bodies and rescues the fatal epilepsy of Lafora disease. PLoS Genet. 7, e1002037.
39. Valles-Ortega J., Duran J., Garcia-Rocha M., et al,. (2011) Neurodegeneration and functional impairments associated with glycogen synthase accumulation in a mouse model of Lafora disease. EMBO Mol. Med. 3, 667-681.
40. Varma S., Shrivastav A., Changela S., and, Khandelwal R. L., (2008) Long-term effects of rapamycin treatment on insulin mediated phosphorylation of Akt/PKB and glycogen synthase activity. Exp. Cell Res. 314, 1281-1291.
41. Vilchez D., Ros S., Cifuentes D., et al,. (2007) Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat. Neurosci. 10, 1407-1413.
42. Wang Y., Ma K., Wang P., Baba O., Zhang H., Parent J. M., Zheng P., Liu Y., and, Minassian B. A,. (2013) Laforin Prevents Stress-Induced Polyglucosan Body Formation and Lafora Disease Progression in Neurons. Mol. Neurobiol. In Press
43. Zahavi E. E., Lieberman J. A., Donnenberg M. S., et al,. (2011) Bundle-forming pilus retraction enhances enteropathogenic Escherichia coli infectivity. Mol. Biol. Cell 22, 2436-2447.