Pharmacotherapeutic management of seizures in patients with Angleman Syndrome

References

• Williams CA, Beaudet AL, Clayton-Smith J, et al. Angelman syndrome 2005: updated consensus for diagnostic criteria. Am J Med Genet A. 2006;140(5):413–418.
   PubMedGoogle Scholar
• Bird LM. Angelman syndrome: review of clinical and molecular aspects. Appl Clin Genet. 2014;7:93–104.
   PubMedGoogle Scholar
• Angelman H. ‘Puppet’children a report on three cases. Dev Med Child Neurol. 1965;7(6):681–688
   Web of Science ®Google Scholar
• Samanta D. *Epilepsy in Angelman syndrome: a scoping review. Brain Dev. 2020;43(1):32–44.
   PubMed Web of Science ®Google Scholar
• Pelc K, Boyd SG, Cheron G, et al. Epilepsy in Angelman syndrome. Seizure. 2008;17(3):211–217.
   PubMed Web of Science ®Google Scholar
• Park SH, Yoon JR, Kim HD, et al. Epilepsy in Korean patients with Angelman syndrome. Korean JPediatr. 2012;55(5):171–176.
   PubMedGoogle Scholar
• Thibert RL, Larson AM, Hsieh DT, et al. Neurologic manifestations of Angelman syndrome. PediatrNeurol. 2013;48:271–279.
   Google Scholar
• Willgoss T, Cassater D, Connor S, et al. Measuring what matters to individuals with Angelman syndrome and their families: Development of a patient-centered disease concept model. Child Psychiatry Human Dev. 2021;52(4):654–668.
   PubMed Web of Science ®Google Scholar
• Borgatti R, Piccinelli P, Passoni D, et al. Peripheral markers of the gamma-aminobutyric acid (GABA)ergic system in Angelman’s syndrome. JChild Neurol. 2003;18(1):21–25.
   PubMed Web of Science ®Google Scholar
• Liljelund P, Handforth A, Homanics GE, et al. GABAA receptor beta3 subunit gene-deficient heterozygous mice show parent-of-origin and gender-related differences in beta3 subunit levels, EEG, and behavior. Brain ResDevBrain Res. 2005;157(2):150–161
   Web of Science ®Google Scholar
• DeLorey TM, Olsen RW. GABA and epileptogenesis: comparing gabrb3 gene-deficient mice with Angelman syndrome in man. Epilepsy Res. 1999;36(2–3):123–132.
   PubMed Web of Science ®Google Scholar
• DeLorey TM, Handforth A, Anagnostaras SG, et al. Mice lacking the β 3 subunit of the GABAA receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman Syndrome. JNeurosci. 1998;18(20):8505–8514.
   PubMed Web of Science ®Google Scholar
• Liljelund P, Ferguson C, Homanics G, et al. Long-term effects of diazepam treatment of epileptic GABAA receptor beta3 subunit knockout mouse in early life. Epilepsy Res. 2005;66(1–3):99–115.
   PubMed Web of Science ®Google Scholar
• Khatri N, Man HY. The autism and Angelman syndrome protein Ube3A/E6AP: The gene, E3 ligase ubiquitination targets and neurobiological functions. FrontMolNeurosci. 2019;12:109.
   Google Scholar
• Kaphzan H, Buffington SA, Jung JI, et al. Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of Angelman syndrome. J Neurosci. 2011;31(48):17637–17648.
   PubMed Web of Science ®Google Scholar
• Dindot SV, Antalffy BA, Bhattacharjee MB, et al. The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum Mol Genet. 2008;17(1):111–118.
   PubMed Web of Science ®Google Scholar
• Fink JJ, Robinson TM, Germain ND, et al. Disrupted neuronal maturation in Angelman syndrome-derived induced pluripotent stem cells. Nat Commun. 2017;8(1):1–14.
   PubMedGoogle Scholar
• Wallace ML, Burette AC, Weinberg RJ, et al. Maternal loss of Ube3a produces an excitatory/inhibitory imbalance through neuron type-specific synaptic defects. Neuron. 2012;74(5):793–800.
   PubMed Web of Science ®Google Scholar
• Laan LA, Renier WO, Arts WF, et al. Evolution of epilepsy and EEG findings in Angelman syndrome. Epilepsia. 1997;38(2):195–199.
   PubMed Web of Science ®Google Scholar
• Buoni S, Grosso S, Pucci L, et al. Diagnosis of Angelman syndrome: clinical and EEG criteria. Brain Dev. 1999;21(5):296–302.
   PubMed Web of Science ®Google Scholar
• Laan LA, Brouwer OF, Begeer CH, et al. The diagnostic value of the EEG in Angelman and rett syndrome at a young age. ElectroencephalogrClinNeurophysiol. 1998;106:404–408.
   PubMedGoogle Scholar
• Leyser M, Penna PS, de Almeida AC, et al. Revisiting epilepsy and the electroencephalogram patterns in Angelman syndrome. NeurolSci. 2014;35:701–705.
   Google Scholar
• Vendrame M, Loddenkemper T, Zarowski M, et al. Analysis of EEG patterns and genotypes in patients with Angelman syndrome. Epilepsy Behav. 2012;23:261–265.
   PubMed Web of Science ®Google Scholar
• Elgersma Y, Sonzogni M. UBE3A reinstatement as a disease‐modifying therapy for Angelman syndrome. Dev Med Child Neurol. 2021;63(7):802–807
   PubMed Web of Science ®Google Scholar
• Yashiro K, Riday TT, Condon KH, et al. Ube3a is required for experience-dependent maturation of the neocortex. Nat Neurosci. 2009;12(6):777–783.
   PubMed Web of Science ®Google Scholar
• Greer PL, Hanayama R, Bloodgood BL, et al. The Angelman syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell. 2010;140(5):704–716.
   PubMed Web of Science ®Google Scholar
• Margolis SS, Salogiannis J, Lipton DM, et al. EphB-mediated degradation of the RhoA GEF ephexin5 relieves a developmental brake on excitatory synapse formation. Cell. 2010;143(3):442–455.
   PubMed Web of Science ®Google Scholar
• Sun AX, Yuan Q, Fukuda M, et al. Potassium channel dysfunction in human neuronal models of Angelman syndrome. Science. 2019;366(6472):1486–1492.
   PubMed Web of Science ®Google Scholar
• Judson MC, Wallace ML, Sidorov MS, et al. GABAergic neuron-specific loss of Ube3a causes Angelman syndrome-like EEG abnormalities and enhances seizure susceptibility. Neuron. 2016;90(1):56–69.
   PubMed Web of Science ®Google Scholar
• Egawa K, Kitagawa K, Inoue K, et al. Decreased tonic inhibition in cerebellar granule cells causes motor dysfunction in a mouse model of Angelman syndrome. SciTranslMed. 2012;4:163ra157.
   PubMed Web of Science ®Google Scholar
• Santini E, Klann E. Genetically dissecting cortical neurons involved in epilepsy in Angelman syndrome. Neuron. 2016;90(1):1–3.
   PubMed Web of Science ®Google Scholar
• Fiumara A, Pittalà A, Cocuzza M, et al. Epilepsy in patients with Angelman syndrome. ItalJPediatr. 2010;36:31–31.
   Web of Science ®Google Scholar
• Van Lierde A, Atza MG, Giardino D, et al. Angelman’s syndrome in the first year of life. DevMedChild Neurol. 1990;32:1011–1016.
   PubMedGoogle Scholar
• Luk HM, Lo IF. Angelman syndrome in Hong Kong Chinese: a 20 years’ experience. EurJMedGenet. 2016;59:315–319.
   Google Scholar
• Cassater D, Bustamante M, Sach-Peltason L, et al. Clinical characterization of epilepsy in children with Angelman syndrome. Pediatr Neurol. 2021;124:42–50.
   PubMed Web of Science ®Google Scholar
• Valente KD, Koiffmann CP, Fridman C, et al. Epilepsy in patients with Angelman syndrome caused by deletion of the chromosome 15q11-13. ArchNeurol. 2006;63:122–128.
   Google Scholar
• Viani F, Romeo A, Viri M, et al. Seizure and EEG patterns in angelman’s syndrome. JChild Neurol. 1995;10(6):467–471.
   PubMed Web of Science ®Google Scholar
• Thibert RL, Conant KD, Braun EK, et al. *Epilepsy in Angelman syndrome: a questionnaire-based assessment of the natural history and current treatment options. Epilepsia. 2009;50(11):2369–2376.
   PubMed Web of Science ®Google Scholar
• Samanta D. Management of lennox-gastaut syndrome beyond childhood: a comprehensive review. Epilepsy Behav. 2021;114:107612.
   PubMed Web of Science ®Google Scholar
• Bakke KA, Howlin P, Retterstøl L, et al. Effect of epilepsy on autism symptoms in Angelman syndrome. MolAutism. 2018;9:2–1. 10.1186/s13229-017-0185-1. eCollection 2018.
   Google Scholar
• Ferlazzo E, Sueri C, Elia M, et al. Reflex seizures in a patient with Angelman syndrome and trisomy 21. NeurolSci. 2016;37:1373–1374.
   Google Scholar
• Pellinen J, Hasan H, Ortiz N, et al. Reflex micturition defecation epilepsy in Angelman syndrome. NeurolClinPract. 2019;9:510–512.
   Google Scholar
• Worden L, Grocott O, Tourjee A, et al. Diazepam for outpatient treatment of nonconvulsive status epilepticus in pediatric patients with Angelman syndrome. Epilepsy Behav. 2018;82:74–80.
   PubMed Web of Science ®Google Scholar
• Elia M. Myoclonic status in nonprogressive encephalopathies: An update. Epilepsia. 2009;50 Suppl 5:41–44.
   PubMed Web of Science ®Google Scholar
• Pollack SF, Grocott OR, Parkin KA, et al. Myoclonus in Angelman syndrome. Epilepsy Behav. 2018;82:170–174.
   PubMed Web of Science ®Google Scholar
• Ferlazzo E, Franceschetti S, Gasparini S, et al. Connectivity measures suggest a sub-cortical generator of myoclonus in Angelman syndrome. Clin Neurophysiol. 2019;130(12):2231–2237.
   PubMed Web of Science ®Google Scholar
• Sueri C, Ferlazzo E, Elia M, et al. Epilepsy and sleep disorders improve in adolescents and adults with Angelman syndrome: a multicenter study on 46 patients. Epilepsy Behav. 2017;75:225–229.
   PubMed Web of Science ®Google Scholar
• Larson AM, Shinnick JE, Shaaya EA, et al. Angelman syndrome in adulthood. AmJMedGenetA. 2015;167A:331–344.
   Google Scholar
• Duis J, Nespeca M, Summers J, et al., *A multidisciplinary approach and consensus statement to establish standards of care for Angelman syndrome. Mol Genet Genomic Med. 10(3): e1843. 2022.
   PubMed Web of Science ®Google Scholar
• Ruggieri M, McShane MA. Parental view of epilepsy in Angelman syndrome: a questionnaire study. ArchDisChild. 1998;79:423–426. 10.1136/adc.79.5.423
   Google Scholar
• Shaaya EA, Grocott OR, Laing O, et al. *Seizure treatment in Angelman syndrome: A case series from the Angelman syndrome clinic at Massachusetts General Hospital. Epilepsy Behav. 2016;60:138–141.
   PubMed Web of Science ®Google Scholar
• Heus KG B, Mous SE, ten Hooven‐radstaake M, et al. An overview of health issues and development in a large clinical cohort of children with Angelman syndrome. Am J Med Genet Part A. 2020;182(1):53–63.
   PubMed Web of Science ®Google Scholar
• Deda G, Caksen H, Kansu A, et al. Toxic hepatitis in a case of Angelman syndrome associated with lennox-gastaut syndrome. GenetCouns. 2004;15:357–361.
   Google Scholar
• Franz DN, Glauser TA, Tudor C, et al. Topiramate therapy of epilepsy associated with angelman’s syndrome. Neurology. 2000;54(5):1185–1188.
   PubMed Web of Science ®Google Scholar
• Dion MH, EJ N Jr, Carmant L, et al. Lamotrigine therapy of epilepsy with angelman’s syndrome. Epilepsia. 2007;48(3):593–596.
   PubMed Web of Science ®Google Scholar
• Kuzniecky R, Ho S, Pan J, et al. Modulation of cerebral GABA by topiramate, lamotrigine, and gabapentin in healthy adults. Neurology. 2002;58(3):368–372.
   PubMed Web of Science ®Google Scholar
• Wang J-F, Sun X, Chen B, et al. Lamotrigine increases gene expression of GABA-A receptor Î23 subunit in primary cultured rat hippocampus cells. Neuropsychopharmacology. 2002;26:415–421.
   PubMed Web of Science ®Google Scholar
• Guberman AH, Besag FM, Brodie MJ, et al. Lamotrigine‐associated rash: risk/benefit considerations in adults and children. Epilepsia. 1999;40(7):985–991.
   PubMed Web of Science ®Google Scholar
• Sugiura C, Ogura K, Ueno M, et al. High-dose ethosuximide for epilepsy in Angelman syndrome: implication of GABA(A) receptor subunit. Neurology. 2001;57(8):1518–1519.
   PubMed Web of Science ®Google Scholar
• Khaleghi F, Nemec EC. Brivaracetam (briviact): a novel adjunctive therapy for partial-onset seizures. Pharm Ther. 2017;42(2):92.
   Google Scholar
• Klein P, Diaz A, Gasalla T, et al. A review of the pharmacology and clinical efficacy of brivaracetam. Clin Pharmacol. 2018;10:1.
   PubMed Web of Science ®Google Scholar
• Yates SL, Fakhoury T, Liang W, et al. An open-label, prospective, exploratory study of patients with epilepsy switching from levetiracetam to brivaracetam. Epilepsy Behav. 2015;52:165–168.
   PubMed Web of Science ®Google Scholar
• Brigo F, Lattanzi S, Nardone R, et al. Intravenous brivaracetam in the treatment of status epilepticus: a systematic review. CNS Drugs. 2019;33(8):771–781.
   PubMed Web of Science ®Google Scholar
• Khan N, Cabo R, Tan W-H, et al. Healthcare burden among individuals with Angelman syndrome: findings from the Angelman syndrome natural history study. Mol Genet Genomic Med. 2019;7(7):e00734.
   PubMed Web of Science ®Google Scholar
• Jensen HS, Nichol K, Lee D, et al. Clobazam and its active metabolite N-desmethylclobazam display significantly greater affinities for α2-versus α1-GABAA–receptor complexes. PLoS One. 2014;9(2):e88456.
   PubMed Web of Science ®Google Scholar
• Samanta D. A scoping review on cannabidiol therapy in tuberous sclerosis: current evidence and perspectives for future development. Epilepsy Behav. 2022;128:108577.
   PubMed Web of Science ®Google Scholar
• Samanta D. Cannabidiol: A review of clinical efficacy and safety in epilepsy. PediatrNeurol. 2019;96:24–29.
   Google Scholar
• Samanta D. Changing landscape of Dravet syndrome management: An overview. Neuropediatrics. 2020;51(2):135–145.
   PubMed Web of Science ®Google Scholar
• Gu B, Zhu M, Glass MR, et al. Cannabidiol attenuates seizures and EEG abnormalities in Angelman syndrome model mice. JClinInvest. 2019;129:5462–5467.
   PubMed Web of Science ®Google Scholar
• Geffrey AL, Pollack SF, Bruno PL, et al. Drug–drug interaction between clobazam and cannabidiol in children with refractory epilepsy. Epilepsia. 2015;56(8):1246–1251.
   PubMed Web of Science ®Google Scholar
• Jensen PK. Felbamate in the treatment of lennox‐gastaut syndrome. Epilepsia. 1994;35(s5):S54–7.
   PubMedGoogle Scholar
• Thakkar K, Billa G, and Rane J, et al. The rise and fall of felbamate as atreatment for partial epilepsy–aplastic anemia and hepatic failure to blame? Expert Rev Neurother. 2015;15(12):1373–1375.
   Web of Science ®Google Scholar
• Ueda Y, Doi T, Tokumaru J, et al. Effect of zonisamide on molecular regulation of glutamate and GABA transporter proteins during epileptogenesis in rats with hippocampal seizures. Mol Brain Res. 2003;116(1–2):1–6.
   PubMedGoogle Scholar
• Yamauchi T, Aikawa H. Efficacy of zonisamide: Our experience. Seizure. 2004;13:S41–8.
   PubMed Web of Science ®Google Scholar
• McLean MJ. Gabapentin. Epilepsia. 1995;36(s2):S73–86.
   PubMedGoogle Scholar
• Grosso S, Coppola G, Cusmai R, et al. Efficacy and tolerability of add‐on lacosamide in children with L ennox‐G astaut syndrome. Acta Neurol Scand. 2014;129(6):420–424.
   PubMed Web of Science ®Google Scholar
• Forrest KM, Young H, Dale RC, et al. Benefit of corticosteroid therapy in Angelman syndrome. JChild Neurol. 2009;24(8):952–958.
   PubMed Web of Science ®Google Scholar
• Kawano O, Egawa K, Shiraishi H. Perampanel for nonepileptic myoclonus in Angelman syndrome. Brain and Development. 2020.
   Google Scholar
• Glauser T, Kluger G, Sachdeo R, et al. Rufinamide for generalized seizures associated with lennox–gastaut syndrome. Neurology. 2008;70(21):1950–1958.
   PubMed Web of Science ®Google Scholar
• Samanta D, Garrity L, Arya R. Refractory and super-refractory status epilepticus. Indian Pediatr. 2020;57(3):239–253.
   PubMed Web of Science ®Google Scholar
• Samanta D. Rescue therapies for seizure emergencies: Current and future landscape. Neurol Sci. 2021;42(10):4017–4027.
   PubMed Web of Science ®Google Scholar
• Kuenzle C, Steinlin M, Wohlrab G, et al. Adverse effects of vigabatrin in Angelman syndrome. Epilepsia. 1998;39(11):1213–1215.
   PubMed Web of Science ®Google Scholar
• Sharp GB, Samanta D, Willis E. Options for pharmacoresistant epilepsy in children: when medications don’t work. Pediatr Ann. 2015;44(2):e43–8.
   PubMed Web of Science ®Google Scholar
• Grocott OR, Herrington KS, Pfeifer HH, et al. Low glycemic index treatment for seizure control in Angelman syndrome: a case series from the center for dietary therapy of epilepsy at the Massachusetts General Hospital. Epilepsy Behav. 2017;68:45–50.
   PubMed Web of Science ®Google Scholar
• Thibert RL, Pfeifer HH, Larson AM, et al. Low glycemic index treatment for seizures in Angelman syndrome. Epilepsia. 2012;53(9):1498–1502.
   PubMed Web of Science ®Google Scholar
• Bi X, Sun J, Ji AX, et al. Potential therapeutic approaches for Angelman syndrome. Expert OpinTherTargets. 2016;20:601–613.
   PubMed Web of Science ®Google Scholar
• Rotaru DC, Mientjes EJ, Elgersma Y. Angelman syndrome: From mouse models to therapy. Neuroscience. 2020;445:172–189.
   PubMed Web of Science ®Google Scholar
• Copping NA, McTighe SM, Fink KD, et al. *Emerging gene and small molecule therapies for the neurodevelopmental disorder Angelman syndrome. Neurotherapeutics. 2021;18(3):1535–1547.
   PubMed Web of Science ®Google Scholar
• Daily JL, Nash K, Jinwal U, et al. Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome. PLoS One. 2011;6(12):e27221.
   PubMed Web of Science ®Google Scholar
• Adhikari A, Copping NA, Beegle J, et al. Functional rescue in an Angelman syndrome model following treatment with lentivector transduced hematopoietic stem cells. Hum Mol Genet. 2021;30(12):1067–1083.
   PubMed Web of Science ®Google Scholar
• Meng L, Person RE, Huang W, et al. Truncation of Ube3a-ATS unsilences paternal Ube3a and ameliorates behavioral defects in the Angelman syndrome mouse model. PLoS Genet. 2013;9(12):e1004039.
   PubMed Web of Science ®Google Scholar
• Huang HS, Allen JA, Mabb AM, et al. Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature. 2011;481(7380):185–189.
   PubMed Web of Science ®Google Scholar
• Meng L, Ward AJ, Chun S, et al. Towards a therapy for Angelman syndrome by targeting a long non-coding RNA. Nature. 2015;518(7539):409–412.
   PubMed Web of Science ®Google Scholar
• Syding LA, Nickl P, Kasparek P, et al. CRISPR/Cas9 epigenome editing potential for rare imprinting diseases: A review. Cells. 2020;9(4):993.
   PubMed Web of Science ®Google Scholar
• Bailus BJ, Segal DJ. The prospect of molecular therapy for Angelman syndrome and other monogenic neurologic disorders. BMC Neurosci. 2014;15(1):76–76.
   PubMed Web of Science ®Google Scholar
• Ciarlone SL, Wang X, Rogawski MA, et al. Effects of the synthetic neurosteroid ganaxolone on seizure activity and behavioral deficits in an Angelman syndrome mouse model. Neuropharmacology. 2017;116:142–150.
   PubMed Web of Science ®Google Scholar
• Ciarlone SL, Grieco JC, D’Agostino DP, et al. Ketone ester supplementation attenuates seizure activity, and improves behavior and hippocampal synaptic plasticity in an Angelman syndrome mouse model. NeurobiolDis. 2016;96:38–46.
   Google Scholar
• Chung L, Bey AL, Towers AJ, et al. Lovastatin suppresses hyperexcitability and seizure in Angelman syndrome model. NeurobiolDis. 2018;110:12–19.
   Google Scholar
• Guzzetti S, Calzari L, Buccarello L, et al. Taurine administration recovers motor and learning deficits in an Angelman syndrome mouse model. IntJMolSci. 2018;19:1088.
   Google Scholar
• Jakaria M, Azam S, Haque ME, et al. Taurine and its analogs in neurological disorders: Focus on therapeutic potential and molecular mechanisms. Redox Biol. 2019;24:101223.
   PubMed Web of Science ®Google Scholar
• Grieco JC, Ciarlone SL, Gieron-Korthals M, et al. An open-label pilot trial of minocycline in children as a treatment for Angelman syndrome. BMC Neurol. 2014;14(1):232–x.
   PubMed Web of Science ®Google Scholar
• Ruiz-Antoran B, Sancho-López A, Cazorla-Calleja R, et al. A randomized placebo controlled clinical trial to evaluate the efficacy and safety of minocycline in patients with Angelman syndrome (A-MANECE study). Orphanet J Rare Dis. 2018;13(1):144.
   PubMedGoogle Scholar
• Bird LM, Ochoa-Lubinoff C, and Tan W-H, et al. The STARS phase 2 study: A randomized controlled trial of gaboxadol in angelman syndrome. Neurology. 2021;96(7):e1024–35 .
   Web of Science ®Google Scholar
• Tones M, Cross M, Simons C, et al. Research protocol: the initiation, design and establishment of the global Angelman syndrome registry. JIntellectDisabilRes. 2018;62:431–443.
   Google Scholar