Pharmacological Interventions to Ameliorate Neuropathological Symptoms in a Mouse Model of Lafora Disease

Molecular Neurobiology

Volumn 53, Issue 2, 2016, Pages 1296-1309

  Berthier, Arnaud ^a   Payá, Miguel ^b   García Cabrero, Ana M ^a   Ballester, Maria Inmaculada ^a   Heredia, Miguel ^a   Serratosa, José M ^a   Sánchez, Marina P ^a   Sanz, Pascual ^a  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

4 Phenylbutyric acid; Lafora disease; Metformin; Pharmacological intervention; Polyglucosan accumulation; Trehalose

Indexed keywords

4 PHENYLBUTYRIC ACID; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; POLYUBIQUITIN; TREHALOSE; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; GLUCAN; NHLRC1 PROTEIN, MOUSE; POLYGLUCOSAN; PROTEIN AGGREGATE; UBIQUITIN PROTEIN LIGASE; UBIQUITINATED PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; MOUSE; MYOCLONUS EPILEPSY; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN AGGREGATION; PROTEOSTASIS DEFICIENCY; ANIMAL; BRAIN; C57BL MOUSE; CELL INCLUSION; COMPLICATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GLIOSIS; HIPPOCAMPUS; KNOCKOUT MOUSE; LAFORA DISEASE; METABOLISM; NERVE DEGENERATION; NEUROPSYCHOLOGICAL TEST; PARASITOLOGY; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GLIOSIS; GLUCANS; HIPPOCAMPUS; INCLUSION BODIES; LAFORA DISEASE; METFORMIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NEUROPSYCHOLOGICAL TESTS; PHENYLBUTYRATES; PROTEIN AGGREGATES; TREHALOSE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATED PROTEINS;

EID: 84958125086     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9091-8     Document Type: Article

References (42)

1. Delgado-Escueta AV (2007) Advances in Lafora progressive myoclonus epilepsy. Curr Neurol Neurosci Rep 7:428–433
2. Monaghan TS, Delanty N (2010) Lafora disease: epidemiology, pathophysiology and management. CNS Drugs 24:549–561
3. Minassian BA, Lee JR, Herbrick JA, Huizenga J, Soder S et al (1998) Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat Genet 20:171–174
4. Serratosa JM, Gomez-Garre P, Gallardo ME, Anta B, de Bernabe DB et al (1999) A novel protein tyrosine phosphatase gene is mutated in progressive myoclonus epilepsy of the Lafora type (EPM2). Hum Mol Genet 8:345–352
5. Chan EM, Young EJ, Ianzano L, Munteanu I, Zhao X et al (2003) Mutations in NHLRC1 cause progressive myoclonus epilepsy. Nat Genet 35:125–127
6. Lohi H, Ianzano L, Zhao XC, Chan EM, Turnbull J et al (2005) Novel glycogen synthase kinase 3 and ubiquitination pathways in progressive myoclonus epilepsy. Hum Mol Genet 14:2727–2736
7. Vilchez D, Ros S, Cifuentes D, Pujadas L, Valles J et al (2007) Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci 10:1407–1413
8. Solaz-Fuster MC, Gimeno-Alcaniz JV, Ros S, Fernandez-Sanchez ME, Garcia-Fojeda B et al (2008) Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMP-activated protein kinase pathway. Hum Mol Genet 17:667–678
9. Liu Y, Wang Y, Wu C, Liu Y, Zheng P (2009) Deletions and missense mutations of EPM2A exacerbate unfolded protein response and apoptosis of neuronal cells induced by endoplasm reticulum stress. Hum Mol Genet 18:2622–2631
10. Vernia S, Rubio T, Heredia M, Rodriguez de Cordoba S, Sanz P (2009) Increased endoplasmic reticulum stress and decreased proteasomal function in Lafora disease models lacking the phosphatase laforin. PLoS One 4:e5907
11. Zeng L, Wang Y, Baba O, Zheng P, Liu Y (2012) Laforin is required for the functional activation of malin in endoplasmic reticulum stress resistance in neuronal cells. FEBS J 279:2467–2478
12. Rao SN, Maity R, Sharma J, Dey P, Shankar SK et al (2010) Sequestration of chaperones and proteasome into Lafora bodies and proteasomal dysfunction induced by Lafora disease-associated mutations of malin. Hum Mol Genet 19:4726–4734
13. Aguado C, Sarkar S, Korolchuk VI, Criado O, Vernia S et al (2010) Laforin, the most common protein mutated in Lafora disease, regulates autophagy. Hum Mol Genet 19:2867–2876
14. Criado O, Aguado C, Gayarre J, Duran-Trio L, Garcia-Cabrero AM et al (2012) Lafora bodies and neurological defects in malin-deficient mice correlate with impaired autophagy. Hum Mol Genet 21:1521–1533
15. Hetz C, Mollereau B (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15:233–249
16. Sinadinos C, Valles-Ortega J, Boulan L, Solsona E, Tevy MF et al (2014) Neuronal glycogen synthesis contributes to physiological aging. Aging Cell 13:935–945
17. Ricobaraza A, Cuadrado-Tejedor M, Perez-Mediavilla A, Frechilla D, Del Rio J et al (2009) Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer’s disease mouse model. Neuropsychopharmacology 34:1721–1732
18. Wiley JC, Meabon JS, Frankowski H, Smith EA, Schecterson LC et al (2010) Phenylbutyric acid rescues endoplasmic reticulum stress-induced suppression of APP proteolysis and prevents apoptosis in neuronal cells. PLoS One 5:e9135
19. Zhou W, Bercury K, Cummiskey J, Luong N, Lebin J et al (2011) Phenylbutyrate up-regulates the DJ-1 protein and protects neurons in cell culture and in animal models of Parkinson disease. J Biol Chem 286:14941–14951
20. Tanaka M, Machida Y, Niu S, Ikeda T, Jana NR et al (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat Med 10:148–154
21. Chen Q, Haddad GG (2004) Role of trehalose phosphate synthase and trehalose during hypoxia: from flies to mammals. J Exp Biol 207:3125–3129
22. Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13:251–262
23. Carling D, Thornton C, Woods A, Sanders MJ (2012) AMP-activated protein kinase: new regulation, new roles? Biochem J 445:11–27
24. Poels J, Spasic MR, Callaerts P, Norga KK (2009) Expanding roles for AMP-activated protein kinase in neuronal survival and autophagy. Bioessays 31:944–952
25. Han Y, Xie N, Cao L, Zhao X, Liu X et al (2011) Adenosine monophosphate-activated protein kinase and peroxisome proliferator-activated receptor gamma coactivator 1alpha signaling provides neuroprotection in status epilepticus in rats. Neurosci Lett 500:133–138
26. Dulovic M, Jovanovic M, Xilouri M, Stefanis L, Harhaji-Trajkovic L et al (2014) The protective role of AMP-activated protein kinase in alpha-synuclein neurotoxicity in vitro. Neurobiol Dis 63:1–11
27. Ashabi G, Khodagholi F, Khalaj L, Goudarzvand M, Nasiri M (2014) Activation of AMP-activated protein kinase by metformin protects against global cerebral ischemia in male rats: interference of AMPK/PGC-1alpha pathway. Metab Brain Dis 29:47–58
28. Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 85:367–370
29. Ogawa N, Hirose Y, Ohara S, Ono T, Watanabe Y (1985) A simple quantitative bradykinesia test in MPTP-treated mice. Res Commun Chem Pathol Pharmacol 50:435–441
30. Stanford SC (2007) The Open Field Test: reinventing the wheel. J Psychopharmacol 21:134–135
31. Luong TN, Carlisle HJ, Southwell A, Patterson PH (2011) Assessment of motor balance and coordination in mice using the balance beam. J Vis Exp 49:2376
32. R-Core-Team (2014) A language and environment for statistical computing. Foundation for Statistical Computing http://www.R-project.org/
33. Valles-Ortega J, Duran J, Garcia-Rocha M, Bosch C, Saez I 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
34. Ortolano S, Vieitez I, Agis-Balboa RC, Spuch C (2014) Loss of GABAergic cortical neurons underlies the neuropathology of Lafora disease. Mol Brain 7:7
35. Turnbull J, DePaoli-Roach AA, Zhao X, Cortez MA, Pencea N et al (2011) PTG depletion removes Lafora bodies and rescues the fatal epilepsy of Lafora disease. PLoS Genet 7:e1002037
36. Pederson BA, Turnbull J, Epp JR, Weaver SA, Zhao X et al (2013) Inhibiting glycogen synthesis prevents Lafora disease in a mouse model. Ann Neurol 74:297–300
37. Turnbull J, Epp JR, Goldsmith D, Zhao X, Pencea N et al (2014) PTG protein depletion rescues malin-deficient Lafora disease in mouse. Ann Neurol 75:442–446
38. Duran J, Gruart A, Garcia-Rocha M, Delgado-Garcia JM, Guinovart JJ (2014) Glycogen accumulation underlies neurodegeneration and autophagy impairment in Lafora disease. Hum Mol Genet 23:3147–3156
39. Carling D, Hardie DG (1989) The substrate and sequence specificity of the AMP-activated protein kinase. Phosphorylation of glycogen synthase and phosphorylase kinase. Biochim Biophys Acta 1012:81–86
40. Tagliabracci VS, Girard JM, Segvich D, Meyer C, Turnbull J et al (2008) Abnormal metabolism of glycogen phosphate as a cause for Lafora disease. J Biol Chem 283:33816–33825
41. DePaoli-Roach AA, Tagliabracci VS, Segvich DM, Meyer CM, Irimia JM et al (2010) Genetic depletion of the malin E3 ubiquitin ligase in mice leads to Lafora bodies and the accumulation of insoluble laforin. J Biol Chem 285:25372–25381
42. Turnbull J, Wang P, Girard JM, Ruggieri A, Wang TJ et al (2010) Glycogen hyperphosphorylation underlies Lafora body formation. Ann Neurol 68:925–933