Serratosa JM, Delgado-Escueta AV, Posada IJ, Shih S, Drury I, Berciano J, et al. The gene for progressive myoclonus epilepsy of the Lafora type maps to chromosome 6q. Hum Mol Genet. 1995;4(9):1657–63.

Article  CAS  PubMed  Google Scholar 

Serratosa JM, Gardiner RM, Lehesjoki AE, Pennacchio LA, Myers RM. The molecular genetic bases of the progressive myoclonus epilepsies. Adv Neurol. 1999;79:383–98.

CAS  PubMed  Google Scholar 

Serratosa JM, Gómez-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(2):345–52.

Article  CAS  PubMed  Google Scholar 

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(11):1251–62.

Article  CAS  PubMed  Google Scholar 

Chan EM, Young EJ, Lanzano L, Munteanu I, Zhao X, Christopoulos CC, et al. Mutations in NHLRC1 cause progressive myoclonus epilepsy. Nat Genet. 2003;35(2):125–7.

Article  CAS  PubMed  Google Scholar 

Gentry MS, Worby CA, Dixon JE. Insights into Lafora disease: malin is an E3 ubiquitin ligase that ubiquitinates and promote the degradation of laforin. Proc Natl Acad Sci USA. 2005;102(24):8501–6.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Worby CA, Gentry MS, Dixon JE. Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem. 2006;281(41):30412–8.

Article  CAS  PubMed  Google Scholar 

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(2):171–4.

Article  CAS  PubMed  Google Scholar 

Sullivan AM, Nitschke S, Steup M, Minassian AB, Nitschke F. Pathogenesis of Lafora disease: transition of soluble glycogen to insoluble polyglucosan. Intl J Mol Sci. 2017;18(8):1743.

Article  Google Scholar 

Nitschke F, Sullivan MA, Wang P, Zhao X, Chown EE, Perri AM, et al. Abnormal glycogen chain length pattern, not hyperphosphorylation, is critical in Lafora disease. EMBO Mol Med. 2017;9(7):906–17.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Nitschke F, Wang P, Schmieder P, Girard JM, Awrey DE, Wang T, et al. Hyperphosphorylation of glucosyl C6 carbons and altered structure of glycogen in the neurodegenerative epilepsy Lafora disease. Cell Metab. 2013;17(5):756–67.

Article  CAS  PubMed  Google Scholar 

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(49):19262–6.

Article  CAS  PubMed  PubMed Central  Google Scholar 

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(49):33816–25.

Article  CAS  PubMed  PubMed Central  Google Scholar 

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(3):274–82.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mitra S, Gumusgoz E, Minassian BA. Lafora disease: current biology and therapeutic approaches. Rev Neruol (Paris). 2022;178(4):315–25.

Article  CAS  Google Scholar 

Gentry MS, Guinovart JJ, Minassian BA, Roach PJ, Serratosa JM. Lafora disease offers a unique window into neuronal glycogen metabolism. J Biol Chem. 2018;293(19):7117–25.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Turnbull J, Tiberia E, Striano P, Genton P, Carpenter S, Ackerley CA, et al. Lafora disease. Epileptic Disord. 2016;18(S2):38–62.

Article  PubMed  PubMed Central  Google Scholar 

Nitschke F, Ahonen SJ, Nitschke S, Mitra S, Minassian BA. Lafora disease - from pathogenesis to treatment strategies. Nat Rev Neurol. 2018;14(10):606–17.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pondrelli F, Muccioli L, Licchetta L, Mostacci B, Zenesini C, Tinuper P, et al. Natural history of Lafora disease: a prognostic systematic review and individual participant data meta-analysis. Orphanet J Rare Dis. 2021;16(1):362.

Article  PubMed  PubMed Central  Google Scholar 

Abubakr A, Wambacq I, Donahue JE, Zappulla R. The presence of polyglucosan bodies in temporal lobe epilepsy: its role and significance. J Clin Neurosci. 2005;12(8):911–4.

Article  CAS  PubMed  Google Scholar 

Duran J, Gruart A, Garcia-Rocha M, Delgado-Garcia JM, Guinovart JJ. Glycogen accumulation underlies neurodegeneration and autophagy impairment in Lafora disease. Hum Mol Genet. 2014;23(12):3147–56.

Article  CAS  PubMed  Google Scholar 

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(4):e1002037.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Turnbull J, Epp JR, Goldsmith D, Zhao X, Pencea N, Wang P, et al. PTG protein depletion rescues malin-deficient Lafora disease in mouse. Ann Neurol. 2014;75(3):442–6.

Article  CAS  PubMed  Google Scholar 

Duran J, Hervera A, Markussen KH, Varea O, López-Soldado I, Sun RC, et al. Astrocytic glycogen accumulation drives the pathophysiology of neurodegeneration in Lafora disease. Brain. 2021;144(8):2349–60.

Article  PubMed  PubMed Central  Google Scholar 

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(2):297–300.

CAS  PubMed  PubMed Central  Google Scholar 

Duran J, Tevy MF, Garcia-Rocha M, Calbó J, Milán M, Guinovart JJ. Deleterious effects of neuronal accumulation of glycogen in flies and mice. EMBO Mol Med. 2012;4(8):719–29.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ahonen S, Nitschke S, Grossman TR, Kordasiewicz H, Wang P, Zhao X, et al. Gys1 antisense therapy rescues neuropathological bases of murine Lafora disease. Brain. 2021;144(10):2985–93.

Article  PubMed  PubMed Central  Google Scholar 

Turnbull J, Wang P, Girard JM, Ruggieri A, Wang TJ, Draginov AG, et al. Glycogen hyperphosphorylation underlies Lafora body formation. Ann Neurol. 2010;68(6):925–33.

Article  CAS  PubMed  Google Scholar 

Baba O. Production of monoclonal antibody that recognizes glycogen and its application for immunohistochemistry. Kokubyo Gakkai Zasshi. 1993;60(2):264–87.

Article  CAS  PubMed  Google Scholar 

Stanback AE, Conroy LR, Young LEA, Hawkinson TR, Markussen KH, Clarke HA, et al. Regional N-glycan and lipid analysis from tissues using MALDI-mass spectrometry imaging. STAR Protoc. 2021;2(1):100304.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hawkinson TR, Sun RC. Matrix-assisted laser desorption/ionization mass spectrometry imaging of glycogen in situ. Methods Mol Biol. 2022;2437:215–28.

Article  CAS  PubMed  Google Scholar 

Sun RC, Young LEA, Bruntz RC, Markussen KH, Zhou Z, Conroy LR, et al. Brain glycogen serves as a critical glucosamine cache required for protein glycosylation. Cell Metab. 2021;33(7):1404-1417.e9.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lopez-Gonzalez I, Viana R, Sanz P, Ferrer I. Inflammation in Lafora disease: evolution with disease progression in laforin and malin knock-out mice. Mol Neurobiol. 2017;54:3119–30.

Article  CAS  PubMed  Google Scholar 

Luna L. AFIP manual of histologic staining methods. New York: EUA; 1986.

Google Scholar 

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(33):25372–81.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Brewer MK, Putaux JL, Rondon A, Uittenbogaard A, Sullivan MA, Gentry MS. Polyglucosan body structure in Lafora disease. Carbohydr Polym. 2020;240:116260.