The phosphatase activity of laforin is dispensable to rescue Epm2a -/- mice from lafora disease

Brain

Volumn 137, Issue 3, 2014, Pages 806-818

  Gayarre, Javier ^a,b   Duran Trío, Lara ^a,b,c   Criado Garcia, Olga ^a,b   Aguado, Carmen ^b,d   Juana López, Lucia ^a   Crespo, Inmaculada ^b,c   Knecht, Erwin ^b,d   Bovolenta, Paola ^b,c   Rodríguez De Córdoba, Santiago ^a,b  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

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

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

autophagy; glycogen phosphorylation; Lafora bodies; Lafora disease; phosphatase activity

Indexed keywords

LAFORIN PROTEIN; PHOSPHATASE; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CODON; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HETEROZYGOTE; HISTOPATHOLOGY; MACROAUTOPHAGY; MEMORY; MOUSE; MUTAGENESIS; MYOCLONUS EPILEPSY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSGENE; WESTERN BLOTTING;

AUTOPHAGY; GLYCOGEN PHOSPHORYLATION; LAFORA BODIES; LAFORA DISEASE; PHOSPHATASE ACTIVITY;

ANIMALS; AUTOPHAGY; DISEASE MODELS, ANIMAL; DUAL-SPECIFICITY PHOSPHATASES; FEMALE; LAFORA DISEASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; PHOSPHORYLATION;

EID: 84894589827     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt353     Document Type: Article

References (55)

1. Aguado C, Sarkar S, Korolchuk VI, Criado O, Vernia S, Boya P, et al. Laforin, the most common protein mutated in Lafora disease, regulates autophagy. Hum Mol Genet 2010; 19: 2867-76.
2. Baraibar MA, Friguet B. Changes of the proteasomal system during the aging process. Prog Mol Biol Transl Sci 2012; 109: 249-75.
3. Baron JC, Marchal G. Cerebral and cardiovascular aging and brain energy metabolism. Studies with positron-emission tomography in man [in French]. Presse Med 1992; 21: 1231-7.
4. Berkovic SF, Andermann F, Carpenter S, Wolfe LS. Progressive myoclonus epilepsies: specific causes and diagnosis. N Engl J Med 1986; 315: 296-305.
5. Borrás C, Stvolinsky S, Ló pez-Grueso R, Fedorova T, Gambini J, Boldyrev A, et al. Low in vivo brain glucose consumption and high oxidative stress in accelerated aging. FEBS Lett 2009 583 2287-93
6. Criado O, Aguado C, Gayarre J, Duran-Trio L, Garcia-Cabrero AM, Vernia S, et al. Lafora bodies and neurological defects in malin-deficient mice correlate with impaired autophagy. Hum Mol Genet 2012; 21: 1521-33.
7. Chan EM, Ackerley CA, Lohi H, Ianzano L, Cortez MA, Shannon P, et al. Laforin preferentially binds the neurotoxic starch-like polyglucosans, which form in its absence in progressive myoclonus epilepsy. Hum Mol Genet 2004; 13: 1117-29.
8. Chan EM, Bulman DE, Paterson AD, Turnbull J, Andermann E, Andermann F, et al. Genetic mapping of a new Lafora progressive myoclonus epilepsy locus (EPM2B) on 6p22. J Med Genet 2003a; 40: 671-5.
9. Chan EM, Young EJ, Ianzano L, Munteanu I, Zhao X, Christopoulos CC, et al. Mutations in NHLRC1 cause progressive myoclonus epilepsy. Nat Genet 2003b; 35: 125-7.
10. DePaoli-Roach AA, Tagliabracci VS, Segvich DM, Meyer CM, Irimia JM, Roach PJ. Genetic depletion of the malin E3 ubiquitin ligase in mice leads to Lafora bodies and the accumulation of insoluble laforin. J Biol Chem 2010; 285: 25372-81.
11. Ferná ndez-Sá nchez ME, Criado-Garća O, Heath Karen E, Garća-Fojeda B, Medrano-Ferná ndez I, Gomez-Garre P, et al. Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Hum Mol Genet 2003 12 3161-71.
12. Ganesh S, Agarwala KL, Ueda K, Akagi T, Shoda K, Usui T, et al. Laforin, defective in the progressive myoclonus epilepsy of Lafora type, is a dual-specificity phosphatase associated with polyribosomes. Hum Mol Genet 2000; 9: 2251-61.
13. Ganesh S, Delgado-Escueta AV, Sakamoto T, Avila MR, Machado-Salas J, Hoshii Y, et al. Targeted disruption of the Epm2a gene causes formation of Lafora inclusion bodies, neurodegeneration, ataxia, myoclonus epilepsy and impaired behavioral response in mice. Hum Mol Genet 2002; 11: 1251-62.
14. Ganesh S, Tsurutani N, Suzuki T, Hoshii Y, Ishihara T, Delgado-Escueta AV, et al. The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem Biophys Res Commun 2004; 313: 1101-9.
15. Gentry M, Worby C, Dixon J. Insights into Lafora disease: Malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin. Proc Natl Acad Sci USA 2005; 102: 8501-6.
16. Gentry MS, Dowen RH, Worby CA, Mattoo S, Ecker JR, Dixon JE. The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J Cell Biol 2007; 178: 477-88.
17. Gentry MS, Romá-Mateo C, Sanz P. Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J 2013; 280: 525-37.
18. Gertz HJ, Cervos-Navarro J, Frydl V, Schultz F. Glycogen accumulation of the aging human brain. Mech Ageing Dev 1985; 31: 25-35.
19. Girard JM, Lê KH, Lederer F. Molecular characterization of laforin, a dual-specificity protein phosphatase implicated in Lafora disease. Biochimie 2006; 88: 1961-71.
20. Harriman DGF, Millar JHD, Stevenson AC. Progressive familial myoclonic epilepsy in three families: its clinical features and pathological basis. Brain 1955; 78: 325-49.
21. Hill D, Summer GK, Waters MD. An automated fluorometric assay for alkaline phosphatase using 3-O-methylfluorescein phosphate. Anal Biochem 1968; 24: 9-17.
22. Knecht E, Criado-Garća O, Aguado C, Gayarre J, Duran-Trio L, Garcia-Cabrero AM, et al. Malin knockout mice support a primary role of autophagy in the pathogenesis of Lafora disease. Autophagy 2012; 8: 701-3.
23. Lafora G, Glueck B. Beitrag zur Histopathologie der myoklonischen epilepsie. Z Gesamte Neurol Psych 1911; 6: 1-14.
24. Lafora GR. Ü ber das Vorkommen amyloider Kö rperchen im Innern der Ganglienzellen: zugleich en Beitrag zum Studium der amyloiden Substanz im Nervensystem. Virchows Arch Pathol 1911; 205: 295-303.
25. Liu Y, Wang Y, Wu C, Liu Y, Zheng P. Deletions and missense mutations of EPM2A exacerbate unfolded protein response and apoptosis of neuronal cells induced by endoplasm reticulum stress. Hum Mol Genet 2009; 18: 2622-31.
26. Lohi H, Ianzano L, Zhao X-C, Chan EM, Turnbull J, Scherer SW, et al. Novel glycogen synthase kinase 3 and ubiquitination pathways in progressive myoclonus epilepsy. Hum Mol Genet 2005; 14: 2727-36.
27. Magistretti PJ, Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 1999; 354: 1155-63.
28. Minassian BA, Lee JR, Herbrick JA, Huizenga J, Soder S, Mungall AJ, et al. Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat Genet 1998; 20: 171-4.
29. Mittal S, Dubey D, Yamakawa K, Ganesh S. Lafora disease proteins malin and laforin are recruited to aggresomes in response to proteasomal impairment. Hum Mol Genet 2007; 16: 753-62.
30. Pederson BA, Turnbull J, Epp JR, Weaver SA, Zhao X, Pencea N, et al. Inhibiting glycogen synthesis prevents Lafora disease in a mouse model. Ann Neurol 2013; 74: 297-300.
31. Puri R, Ganesh S. Laforin in autophagy: a possible link between carbohydrate and protein in Lafora disease? Autophagy 2010; 6: 1229-31.
32. Puri R, Ganesh S. Autophagy defects in Lafora disease: cause or consequence? Autophagy 2012; 8: 289-90.
33. Puri R, Suzuki T, Yamakawa K, Ganesh S. Dysfunctions in endosomal-lysosomal and autophagy pathways underlie neuropathology in a mouse model for Lafora disease. Hum Mol Genet 2012; 21: 175-84.
34. Roach PJ. Are there errors in glycogen biosynthesis and is laforin a repair enzyme? FEBS Lett 2011; 585: 3216-8.
35. Rubinsztein DC, Mariñ o G, Kroemer G. Autophagy and aging. Cell 2011; 146: 682-95.
36. Scullion GA, Kendall DA, Marsden CA, Sunter D, Pardon MC. Chronic treatment with the-2-adrenoceptor antagonist fluparoxan prevents age-related deficits in spatial working memory in APP-PS1 transgenic mice without altering b-amyloid plaque load or astrocytosis. Neuropharmacology 2011; 60: 223-34.
37. Serratosa JM, Gó mez-Garre P, Gallardo ME, Anta B, de Bernabé DB, Lindhout D, et al. A novel protein tyrosine phosphatase gene is mutated in progressive myoclonus epilepsy of the Lafora type (EPM2). Hum Mol Genet 1999; 8: 345-52.
38. Sharma J, Mukherjee D, Rao SN, Iyengar S, Shankar SK, Satishchandra P, et al. Neuronatin-mediated aberrant calcium signaling and endoplasmic reticulum stress underlie neuropathology in Lafora disease. J Biol Chem 2013; 288: 9482-90.
39. Sharma J, Mulherkar S, Mukherjee D, Jana NR. Malin regulates Wnt signaling pathway through degradation of Dishevelled2. J Biol Chem 2012; 287: 6830-9.
40. Solaz-Fuster MC, Gimeno-Alcañ iz JV, Ros S, Fernandez-Sanchez ME, Garcia-Fojeda B, Criado-Garcia O, et al. Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMPactivated protein kinase pathway. Hum Mol Genet 2008; 17: 667-78.
41. Tagliabracci VS, Girard JM, Segvich D, Meyer C, Turnbull J, Zhao X, et al. Abnormal metabolism of glycogen phosphate as a cause for Lafora disease. J Biol Chem 2008; 283: 33816-25.
42. Tagliabracci VS, Heiss C, Karthik C, Contreras CJ, Glushka J, Ishihara M, et al. Phosphate incorporation during glycogen synthesis and Lafora disease. Cell Metab 2011; 13: 274-82.
43. Tagliabracci VS, Turnbull J, Wang W, Girard JM, Zhao X, Skurat AV, et al. Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc Natl Acad Sci USA 2007; 104: 19262-6.
44. Tiberia E, Turnbull J, Wang T, Ruggieri A, Zhao XC, Pencea N, et al. Increased laforin and laforin binding to glycogen underlie Lafora body formation in malin-deficient Lafora disease. J Biol Chem 2012; 287: 25650-9.
45. Turnbull J, DePaoli-Roach AA, Zhao X, Cortez MA, Pencea N, Tiberia E, et al. PTG depletion removes Lafora bodies and rescues the fatal epilepsy of Lafora disease. Plos Genet 2011; 7: e1002037.
46. Turnbull J, Wang P, Girard JM, Ruggieri A, Wang TJ, Draginov AG, et al. Glycogen hyperphosphorylation underlies Lafora body formation. Ann Neurol 2010; 68: 925-33.
47. Valles-Ortega J, Duran J, Garcia-Rocha M, Bosch C, Saez I, Pujadas L, et al. Neurodegeneration and functional impairments associated with glycogen synthase accumulation in a mouse model of Lafora disease. EMBO Mol Med 2011; 3: 667-81.
48. Vernia S, Rubio T, Heredia M, Rodr?́guez de Có rdoba S, Sanz P. Increased endoplasmic reticulum stress and Decreased proteasomal function in Lafora disease models lacking the phosphatase laforin. PLoS One 2009; 4: e5907.
49. Vilchez D, Ros S, Cifuentes D, Pujadas L, Valles J, Garcia-Fojeda B, et al. Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci 2007; 10: 1407-13.
50. Wang J, Stuckey JA, Wishart MJ, Dixon JE. A Unique carbohydrate binding domain targets the Lafora disease phosphatase to glycogen. J Biol Chem 2002; 277: 2377-80.
51. Wang W, Roach PJ. Glycogen and related polysaccharides inhibit the laforin dual-specificity protein phosphatase. Biochem Biophys Res Commun 2004; 325: 726-30.
52. Worby CA, Gentry MS, Dixon JE. Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 2006; 281: 30412-8.
53. Worby CA, Gentry MS, Dixon JE. Malin decreases glycogen accumulation by promoting the degradation of protein targeting to glycogen (PTG). J Biol Chem 2008; 283: 4069-76.
54. Yokoi S, Austin J, Witmer F, Sakai M. Studies in myoclonus epilepsy (Lafora body form) I. Isolation and preliminary characterization of Lafora bodies in two cases. Arch Neurol 1968; 19: 15-33.
55. Zeng L, Wang Y, Baba O, Zheng P, Liu Y, Liu Y. Laforin is required for the functional activation of malin in endoplasmic reticulum stress resistance in neuronal cells. FEBS J 2012; 279: 2467-78.