Pathogenesis and new candidate treatments for infantile spasms and early life epileptic encephalopathies: A view from preclinical studies

Neurobiology of Disease

Volumn 79, Issue , 2015, Pages 135-149

  Galanopoulou, Aristea S ^a   Moshé, Solomon L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Arx; Cognition; Dravet syndrome; Epilepsy; GABA; MTOR; Multiple hit model; NMDA; Sodium channels; SUDEP; Tetrodotoxin; West syndrome

Indexed keywords

ANTICONVULSIVE AGENT; BETAMETHASONE; GAMMA BUTYROLACTONE; N METHYL DEXTRO ASPARTIC ACID;

ACUTE DISEASE; BEHAVIOR DISORDER; BRAIN DISEASE; CDKL5 GENE; CHRONIC DISEASE; COGNITIVE DEFECT; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; DISEASE MODEL; DOWN SYNDROME; EARLY ONSET AND INFANTILE EPILEPTIC ENCEPHALOPATHY; EIEE13 GENE; EIEE15 GENE; EIEE17 GENE; EIEE18 GENE; EIEE2 GENE; EIEE4 GENE; EIEE7 GENE; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; GENE; GENE DISRUPTION; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC MODEL; GNAO1 GENE; HUMAN; INFANT DISEASE; INFANTILE SPASM; KCNQ2 GENE; MEF2C GENE; MOLECULAR PATHOLOGY; NERVE CELL DIFFERENTIATION; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PERINATAL DRUG EXPOSURE; PERINATAL STRESS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REVIEW; RODENT; SCN8A GENE; SEIZURE; SEVERE MYOCLONIC EPILEPSY IN INFANCY; ST3GAL3 GENE; STXBP1 GENE; SZT2 GENE; X CHROMOSOME LINKED DISORDER; ANIMAL; EPILEPSIES, MYOCLONIC; INFANT; PATHOPHYSIOLOGY; SPASMS, INFANTILE;

ANIMALS; DISEASE MODELS, ANIMAL; EPILEPSIES, MYOCLONIC; HUMANS; INFANT; SPASMS, INFANTILE;

EID: 84929410637     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.04.015     Document Type: Review

References (185)

1. Aarts J.H., Binnie C.D., Smit A.M., Wilkins A.J. Selective cognitive impairment during focal and generalized epileptiform EEG activity. Brain 1984, 107(Pt 1):293-308.
2. Akman O., Briggs S.W., Galanopoulou A.S. Long-term follow up of the multiple-hit model of symptomatic infantile spasms. Epilepsy Curr. 2012, 13:147.
3. Akman O., Moshe S.L., Galanopoulou A.S. Sex-specific consequences of early life seizures. Neurobiol. Dis. 2014, 72(Pt B):153-166.
4. Amendola E., Zhan Y., Mattucci C., Castroflorio E., Calcagno E., Fuchs C., et al. Mapping pathological phenotypes in a mouse model of CDKL5 disorder. PLoS One 2014, 9:e91613.
5. Auerbach D.S., Jones J., Clawson B.C., Offord J., Lenk G.M., Ogiwara I., et al. Altered cardiac electrophysiology and SUDEP in a model of Dravet syndrome. PLoS One 2013, 8:e77843.
6. Auvin S., Lamblin M.D., Pandit F., Vallee L., Bouvet-Mourcia A. Infantile epileptic encephalopathy with late-onset spasms: report of 19 patients. Epilepsia 2010, 51:1290-1296.
7. Avishai-Eliner S., Brunson K.L., Sandman C.A., Baram T.Z. Stressed-out, or in (utero)?. Trends Neurosci. 2002, 25:518-524.
8. Baraban S.C., Dinday M.T., Hortopan G.A. Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment. Nat. Commun. 2013, 4:2410.
9. Baram T.Z. Pathophysiology of massive infantile spasms: perspective on the putative role of the brain adrenal axis. Ann. Neurol. 1993, 33:231-236.
10. Baram T.Z., Lerner S.P. Ontogeny of corticotropin releasing hormone gene expression in rat hypothalamus - comparison with somatostatin. Int. J. Dev. Neurosci. 1991, 9:473-478.
11. Baram T.Z., Schultz L. Corticotropin-releasing hormone is a rapid and potent convulsant in the infant rat. Brain Res. Dev. Brain Res. 1991, 61:97-101.
12. Baram T.Z., Mitchell W.G., Snead O.C., Horton E.J., Saito M. Brain-adrenal axis hormones are altered in the CSF of infants with massive infantile spasms. Neurology 1992, 42:1171-1175.
13. Baram T.Z., Mitchell W.G., Brunson K., Haden E. Infantile spasms: hypothesis-driven therapy and pilot human infant experiments using corticotropin-releasing hormone receptor antagonists. Dev. Neurosci. 1999, 21:281-289.
14. Barcia G., Barnerias C., Rio M., Siquier-Pernet K., Desguerre I., Colleaux L., et al. A novel mutation in STXBP1 causing epileptic encephalopathy (late onset infantile spasms) with partial respiratory chain complex IV deficiency. Eur. J. Med. Genet. 2013, 56:683-685.
15. Barcia G., Chemaly N., Gobin S., Milh M., Van Bogaert P., Barnerias C., et al. Early epileptic encephalopathies associated with STXBP1 mutations: could we better delineate the phenotype?. Eur. J. Med. Genet. 2014, 57:15-20.
16. Basel-Vanagaite L., Hershkovitz T., Heyman E., Raspall-Chaure M., Kakar N., Smirin-Yosef P., et al. Biallelic SZT2 mutations cause infantile encephalopathy with epilepsy and dysmorphic corpus callosum. Am. J. Hum. Genet. 2013, 93:524-529.
17. Baumbach H.D., Chow K.L. Visuocortical epileptiform discharges in rabbits: differential effects on neuronal development in the lateral geniculate nucleus and superior colliculus. Brain Res. 1981, 209:61-76.
18. Beguin S., Crepel V., Aniksztejn L., Becq H., Pelosi B., Pallesi-Pocachard E., et al. An epilepsy-related ARX polyalanine expansion modifies glutamatergic neurons excitability and morphology without affecting GABAergic neurons development. Cereb. Cortex 2013, 23:1484-1494.
19. Berg A.T., Berkovic S.F., Brodie M.J., Buchhalter J., Cross J.H., van Emde Boas W., et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 2010, 51:676-685.
20. Best T.K., Siarey R.J., Galdzicki Z. Ts65Dn, a mouse model of Down syndrome, exhibits increased GABAB-induced potassium current. J. Neurophysiol. 2007, 97:892-900.
21. Bi W., Drake C.J., Schwarz J.J. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev. Biol. 1999, 211:255-267.
22. Binnie C.D., Kasteleijn-Nolst Trenite D.G., Smit A.M., Wilkins A.J. Interactions of epileptiform EEG discharges and cognition. Epilepsy Res. 1987, 1:239-245.
23. Blanchard M.G., Willemsen M.H., Walker J.B., Dib-Hajj S.D., Waxman S.G., Jongmans M.C., et al. De novo gain-of-function and loss-of-function mutations of SCN8A in patients with intellectual disabilities and epilepsy. J. Med. Genet. 2015, 52:330-337.
24. Bonneau D., Toutain A., Laquerriere A., Marret S., Saugier-Veber P., Barthez M.A., et al. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann. Neurol. 2002, 51:340-349.
25. Boutry-Kryza N., Labalme A., Ville D., de Bellescize J., Touraine R., Prieur F., et al. Molecular characterization of a cohort of 73 patients with infantile spasms syndrome. Eur. J. Med. Genet. 2015, 58:51-58.
26. Briggs S.W., Mowrey W., Hall C.B., Galanopoulou A.S. CPP-115, a vigabatrin analogue, decreases spasms in the multiple-hit rat model of infantile spasms. Epilepsia 2014, 55:94-102.
27. Cao D., Ohtani H., Ogiwara I., Ohtani S., Takahashi Y., Yamakawa K., et al. Efficacy of stiripentol in hyperthermia-induced seizures in a mouse model of Dravet syndrome. Epilepsia 2012, 53:1140-1145.
28. Cardamone M., Flanagan D., Mowat D., Kennedy S.E., Chopra M., Lawson J.A. Mammalian target of rapamycin inhibitors for intractable epilepsy and subependymal giant cell astrocytomas in tuberous sclerosis complex. J. Pediatr. 2014, 164:1195-1200.
29. Carvill G.L., Heavin S.B., Yendle S.C., McMahon J.M., O'Roak B.J., Cook J., et al. Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet. 2013, 45:825-830.
30. Chachua T., Yum M.S., Veliskova J., Velisek L. Validation of the rat model of cryptogenic infantile spasms. Epilepsia 2011, 52:1666-1677.
31. Chan C.H., Godinho L.N., Thomaidou D., Tan S.S., Gulisano M., Parnavelas J.G. Emx1 is a marker for pyramidal neurons of the cerebral cortex. Cereb. Cortex 2001, 11:1191-1198.
32. Chan K.F., Jia Z., Murphy P.A., Burnham W.M., Cortez M.A., Snead O.C. Learning and memory impairment in rats with chronic atypical absence seizures. Exp. Neurol. 2004, 190:328-336.
33. Chan K.F., Burnham W.M., Jia Z., Cortez M.A., Snead O.C. GABAB receptor antagonism abolishes the learning impairments in rats with chronic atypical absence seizures. Eur. J. Pharmacol. 2006, 541:64-72.
34. Cheah C.S., Yu F.H., Westenbroek R.E., Kalume F.K., Oakley J.C., Potter G.B., et al. Specific deletion of NaV1.1 sodium channels in inhibitory interneurons causes seizures and premature death in a mouse model of Dravet syndrome. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14646-14651.
35. Chen C., Westenbroek R.E., Xu X., Edwards C.A., Sorenson D.R., Chen Y., et al. Mice lacking sodium channel beta1 subunits display defects in neuronal excitability, sodium channel expression, and nodal architecture. J. Neurosci. 2004, 24:4030-4042.
36. Chow K.L., Baumbach H.D., Glanzman D.L. Abnormal development of lateral geniculate neurons in rabbit subjected to either eyelid closure or corticofugal paroxysmal discharges. Brain Res. 1978, 146:151-158.
37. Chu-Shore C.J., Major P., Camposano S., Muzykewicz D., Thiele E.A. The natural history of epilepsy in tuberous sclerosis complex. Epilepsia 2010, 51:1236-1241.
38. Claes L., Del-Favero J., Ceulemans B., Lagae L., Van Broeckhoven C., De Jonghe P. De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy. Am. J. Hum. Genet. 2001, 68:1327-1332.
39. Clancy B., Darlington R.B., Finlay B.L. Translating developmental time across mammalian species. Neuroscience 2001, 105:7-17.
40. Coleman M. Infantile spasms associated with 5-hydroxytryptophan administration in patients with Down's syndrome. Neurology 1971, 21:911-919.
41. Cortez M.A., McKerlie C., Snead O.C. A model of atypical absence seizures: EEG, pharmacology, and developmental characterization. Neurology 2001, 56:341-349.
42. Cortez M.A., Shen L., Wu Y., Aleem I.S., Trepanier C.H., Sadeghnia H.R., et al. Infantile spasms and Down syndrome: a new animal model. Pediatr. Res. 2009, 65:499-503.
43. Curatolo P., D'Argenzio L., Cerminara C., Bombardieri R. Management of epilepsy in tuberous sclerosis complex. Expert. Rev. Neurother. 2008, 8:457-467.
44. Dobbing J. The later growth of the brain and its vulnerability. Pediatrics 1974, 53:2-6.
45. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 1979, 3:79-83.
46. Dobyns W.B., Berry-Kravis E., Havernick N.J., Holden K.R., Viskochil D. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia. Am. J. Med. Genet. 1999, 86:331-337.
47. Dravet C., Oguni H. Dravet syndrome (severe myoclonic epilepsy in infancy). Handb. Clin. Neurol. 2013, 111:627-633.
48. Dulac O., Bast T., Dalla Bernardina B., Gaily E., Neville B. Infantile spasms: toward a selective diagnostic and therapeutic approach. Epilepsia 2010, 51:2218-2219. (author reply 2221).
49. Dutton S.B., Sawyer N.T., Kalume F., Jumbo-Lucioni P., Borges K., Catterall W.A., et al. Protective effect of the ketogenic diet in Scn1a mutant mice. Epilepsia 2011, 52:2050-2056.
50. Edvardson S., Baumann A.M., Muhlenhoff M., Stephan O., Kuss A.W., Shaag A., et al. West syndrome caused by ST3Gal-III deficiency. Epilepsia 2013, 54:e24-e27.
51. Epi4K.Consortium, Epilepsy Phenome/Genome Project, Allen A.S., Berkovic S.F., Cossette P., Delanty N., et al. "De novo mutations in epileptic encephalopathies". Nature 2013, 501:217-221.
52. Escayg A., Goldin A.L. Sodium channel SCN1A and epilepsy: mutations and mechanisms. Epilepsia 2010, 51:1650-1658.
53. Escayg A., MacDonald B.T., Meisler M.H., Baulac S., Huberfeld G., An-Gourfinkel I., et al. Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat. Genet. 2000, 24:343-345.
54. Estacion M., O'Brien J.E., Conravey A., Hammer M.F., Waxman S.G., Dib-Hajj S.D., et al. A novel de novo mutation of SCN8A (Nav1.6) with enhanced channel activation in a child with epileptic encephalopathy. Neurobiol. Dis. 2014, 69:117-123.
55. EuroEPINOMICS-RES Consortium Epilepsy Phenome/Genome Project and Epi4K Consortium De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am. J. Hum. Genet. 2014, 95:360-370.
56. Facchinetti F., Nalin A., Petraglia F., Galli V., Genazzani A.R. Reduced ACTH, while normal beta-endorphin CSF levels in early epileptic encephalopathies. Peptides 1985, 6:31-33.
57. Falcone M., Yariz K.O., Ross D.B., Foster J., Menendez I., Tekin M. An amino acid deletion inSZT2 in a family with non-syndromic intellectual disability. PLoS One 2013, 8:e82810.
58. Frankel W.N., Yang Y., Mahaffey C.L., Beyer B.J., O'Brien T.P. Szt2, a novel gene for seizure threshold in mice. Genes Brain Behav. 2009, 8:568-576.
59. Friocourt G., Parnavelas J.G. Mutations in ARX result in several defects involving GABAergic neurons. Front. Cell. Neurosci. 2010, 4:4.
60. Frost J.D., Hrachovy R.A. Pathogenesis of infantile spasms: a model based on developmental desynchronization. J. Clin. Neurophysiol. 2005, 22:25-36.
61. Frost J.D., Lee C.L., Hrachovy R.A., Swann J.W. High frequency EEG activity associated with ictal events in an animal model of infantile spasms. Epilepsia 2011, 52:53-62.
62. Frost J.D., Lee C.L., Le J.T., Hrachovy R.A., Swann J.W. Interictal high frequency oscillations in an animal model of infantile spasms. Neurobiol. Dis. 2012, 46:377-388.
63. Fujiwara T., Sugawara T., Mazaki-Miyazaki E., Takahashi Y., Fukushima K., Watanabe M., et al. Mutations of sodium channel alpha subunit type 1 (SCN1A) in intractable childhood epilepsies with frequent generalized tonic-clonic seizures. Brain 2003, 126:531-546.
64. Galanopoulou A.S. Basic mechanisms of catastrophic epilepsy - overview from animal models. Brain Dev. 2013, 35:748-756.
65. Galanopoulou A.S., Moshe S.L. In search of epilepsy biomarkers in the immature brain: goals, challenges and strategies. Biomark. Med 2011, 5:615-628.
66. Galanopoulou A.S., Bojko A., Lado F., Moshe S.L. The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev. 2000, 22:279-295.
67. Galanopoulou A.S., Gorter J.A., Cepeda C. Finding a better drug for epilepsy: the mTOR pathway as an antiepileptogenic target. Epilepsia 2012, 53:1119-1130.
68. Gheyara A.L., Ponnusamy R., Djukic B., Craft R.J., Ho K., Guo W., et al. Tau reduction prevents disease in a mouse model of Dravet syndrome. Ann. Neurol. 2014, 76:443-456.
69. Go C.Y., Mackay M.T., Weiss S.K., Stephens D., Adams-Webber T., Ashwal S., et al. Evidence-based guideline update: medical treatment of infantile spasms. Report of the Guideline Development Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology 2012, 78:1974-1980.
70. Goldberg-Stern H., Strawsburg R.H., Patterson B., Hickey F., Bare M., Gadoth N., et al. Seizure frequency and characteristics in children with Down syndrome. Brain Dev. 2001, 23:375-378.
71. Gottlieb A., Keydar I., Epstein H.T. Rodent brain growth stages: an analytical review. Biol. Neonate 1977, 32:166-176.
72. Hager T., Maroteaux G., Pont P., Julsing J., van Vliet R., Stiedl O. Munc18-1 haploinsufficiency results in enhanced anxiety-like behavior as determined by heart rate responses in mice. Behav. Brain Res. 2014, 260:44-52.
73. Han S., Tai C., Westenbroek R.E., Yu F.H., Cheah C.S., Potter G.B., et al. Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature 2012, 489:385-390.
74. Heiskala H. CSF ACTH and beta-endorphin in infants with West syndrome and ACTH therapy. Brain Dev. 1997, 19:339-342.
75. Hernan A.E., Alexander A., Jenks K.R., Barry J., Lenck-Santini P.P., Isaeva E., et al. Focal epileptiform activity in the prefrontal cortex is associated with long-term attention and sociability deficits. Neurobiol. Dis. 2014, 63:25-34.
76. Hernan A.E., Alexander A., Lenck-Santini P.P., Scott R.C., Holmes G.L. Attention deficit associated with early life interictal spikes in a rat model is improved with ACTH. PLoS One 2014, 9:e89812.
77. Hong A.M., Turner Z., Hamdy R.F., Kossoff E.H. Infantile spasms treated with the ketogenic diet: prospective single-center experience in 104 consecutive infants. Epilepsia 2010, 51:1403-1407.
78. Hrachovy R.A., Frost J.D., Kellaway P. Hypsarrhythmia: variations on the theme. Epilepsia 1984, 25:317-325.
79. Insel T.R., Battaglia G., De Fairbanks D.W., Souza E.B. The ontogeny of brain receptors for corticotropin-releasing factor and the development of their functional association with adenylate cyclase. J. Neurosci. 1988, 8:4151-4158.
80. Jequier Gygax M., Klein B.D., White H.S., Kim M., Galanopoulou A.S. Efficacy and tolerability of the galanin analog NAX 5055 in the multiple-hit rat model of symptomatic infantile spasms. Epilepsy Res. 2014, 108:98-108.
81. Kabova R., Liptakova S., Slamberova R., Pometlova M., Velisek L. Age-specific N-methyl-D-aspartate-induced seizures: perspectives for the West syndrome model. Epilepsia 1999, 40:1357-1369.
82. Kalscheuer V.M., Tao J., Donnelly A., Hollway G., Schwinger E., Kubart S., et al. Disruption of the serine/threonine kinase 9 gene causes severe X-linked infantile spasms and mental retardation. Am. J. Hum. Genet. 2003, 72:1401-1411.
83. Kalume F., Yu F.H., Westenbroek R.E., Scheuer T., Catterall W.A. Reduced sodium current in Purkinje neurons from Nav1.1 mutant mice: implications for ataxia in severe myoclonic epilepsy in infancy. J. Neurosci. 2007, 27:11065-11074.
84. Kalume F., Westenbroek R.E., Cheah C.S., Yu F.H., Oakley J.C., Scheuer T., et al. Sudden unexpected death in a mouse model of Dravet syndrome. J. Clin. Invest. 2013, 123:1798-1808.
85. Kasteleijn-Nolst Trenite D.G., Vermeiren R. The impact of subclinical epileptiform discharges on complex tasks and cognition: relevance for aircrew and air traffic controllers. Epilepsy Behav. 2005, 6:31-34.
86. Kasteleijn-Nolst Trenite D.G., Riemersma J.B., Binnie C.D., Smit A.M., Meinardi H. The influence of subclinical epileptiform EEG discharges on driving behaviour. Electroencephalogr. Clin. Neurophysiol. 1987, 67:167-170.
87. Kato M., Dobyns W.B. X-linked lissencephaly with abnormal genitalia as a tangential migration disorder causing intractable epilepsy: proposal for a new term, "interneuronopathy". J. Child Neurol. 2005, 20:392-397.
88. Kato M., Das S., Petras K., Sawaishi Y., Dobyns W.B. Polyalanine expansion of ARX associated with cryptogenic West syndrome. Neurology 2003, 61:267-276.
89. Kearney J.A., Buchner D.A., De Haan G., Adamska M., Levin S.I., Furay A.R., et al. Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a (Na(v)1.6). Hum. Mol. Genet. 2002, 11:2765-2775.
90. Kehrl J.M., Sahaya K., Dalton H.M., Charbeneau R.A., Kohut K.T., Gilbert K., et al. Gain-of-function mutation in Gnao1: a murine model of epileptiform encephalopathy (EIEE17)?. Mamm. Genome 2014, 25:202-210.
91. Kerrigan J.F., Shields W.D., Nelson T.Y., Bluestone D.L., Dodson W.E., Bourgeois B.F., et al. Ganaxolone for treating intractable infantile spasms: a multicenter, open-label, add-on trial. Epilepsy Res. 2000, 42:133-139.
92. Khan O.I., Zhao Q., Miller F., Holmes G.L. Interictal spikes in developing rats cause long-standing cognitive deficits. Neurobiol. Dis. 2010, 39:362-371.
93. Kitamura K., Itou Y., Yanazawa M., Ohsawa M., Suzuki-Migishima R., Umeki Y., et al. Three human ARX mutations cause the lissencephaly-like and mental retardation with epilepsy-like pleiotropic phenotypes in mice. Hum. Mol. Genet. 2009, 18:3708-3724.
94. Kiwamoto T., Brummet M.E., Wu F., Motari M.G., Smith D.F., Schnaar R.L., et al. Mice deficient in the St3gal3 gene product alpha2,3 sialyltransferase (ST3Gal-III) exhibit enhanced allergic eosinophilic airway inflammation. J. Allergy Clin. Immunol. 2014, 133:240-247. (e241-243).
95. Kleen J.K., Scott R.C., Holmes G.L., Lenck-Santini P.P. Hippocampal interictal spikes disrupt cognition in rats. Ann. Neurol. 2010, 67:250-257.
96. Krueger D.A., Wilfong A.A., Holland-Bouley K., Anderson A.E., Agricola K., Tudor C., et al. Everolimus treatment of refractory epilepsy in tuberous sclerosis complex. Ann. Neurol. 2013, 74:679-687.
97. Kubova H., Mares P. Vigabatrin but not valproate prevents development of age-specific flexion seizures induced by N-methyl-D-aspartate (NMDA) in immature rats. Epilepsia 2010, 51:469-472.
98. Kumar D., Boehm U. Genetic dissection of puberty in mice. Exp. Physiol. 2013, 98:1528-1534.
99. Lado F.A., Moshe S.L. Role of subcortical structures in the pathogenesis of infantile spasms: what are possible subcortical mediators?. Int. Rev. Neurobiol. 2002, 49:115-140.
100. Langlais P.J., Wardlow M.L., Yamamoto H. Changes in CSF neurotransmitters in infantile spasms. Pediatr. Neurol. 1991, 7:440-445.
101. Lee C.L., Frost J.D., Swann J.W., Hrachovy R.A. A new animal model of infantile spasms with unprovoked persistent seizures. Epilepsia 2008, 49:298-307.
102. Lemke J.R., Hendrickx R., Geider K., Laube B., Schwake M., Harvey R.J., et al. GRIN2B mutations in West syndrome and intellectual disability with focal epilepsy. Ann. Neurol. 2014, 75:147-154.
103. Li H., Radford J.C., Ragusa M.J., Shea K.L., McKercher S.R., Zaremba J.D., et al. Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation in vivo. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9397-9402.
104. Lin Q., Schwarz J., Bucana C., Olson E.N. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 1997, 276:1404-1407.
105. Liptakova S., Velisek L., Veliskova J., Moshe S.L. Effect of ganaxolone on flurothyl seizures in developing rats. Epilepsia 2000, 41:788-793.
106. Lux A.L., Edwards S.W., Hancock E., Johnson A.L., Kennedy C.R., Newton R.W., et al. The United Kingdom Infantile Spasms Study (UKISS) comparing hormone treatment with vigabatrin on developmental and epilepsy outcomes to age 14months: a multicentre randomised trial. Lancet Neurol. 2005, 4:712-717.
107. Mackay M.T., Weiss S.K., Adams-Webber T., Ashwal S., Stephens D., Ballaban-Gill K., et al. Practice parameter: medical treatment of infantile spasms: report of the American Academy of Neurology and the Child Neurology Society. Neurology 2004, 62:1668-1681.
108. Mares P., Velisek L. N-methyl-D-aspartate (NMDA)-induced seizures in developing rats. Brain Res. Dev. Brain Res. 1992, 65:185-189.
109. Mari F., Azimonti S., Bertani I., Bolognese F., Colombo E., Caselli R., et al. CDKL5 belongs to the same molecular pathway of MeCP2 and it is responsible for the early-onset seizure variant of Rett syndrome. Hum. Mol. Genet. 2005, 14:1935-1946.
110. Marini C., Scheffer I.E., Nabbout R., Suls A., De Jonghe P., Zara F., et al. The genetics of Dravet syndrome. Epilepsia 2011, 52(Suppl. 2):24-29.
111. Marsh E., Fulp C., Gomez E., Nasrallah I., Minarcik J., Sudi J., et al. Targeted loss of Arx results in a developmental epilepsy mouse model and recapitulates the human phenotype in heterozygous females. Brain 2009, 132:1563-1576.
112. Martin M.S., Dutt K., Papale L.A., Dube C.M., Dutton S.B., de Haan G., et al. Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J. Biol. Chem. 2010, 285:9823-9834.
113. Michaud J.L., Lachance M., Hamdan F.F., Carmant L., Lortie A., Diadori P., et al. The genetic landscape of infantile spasms. Hum. Mol. Genet. 2014, 23:4846-4858.
114. Mistry A.M., Thompson C.H., Miller A.R., Vanoye C.G., George A.L., Kearney J.A. Strain- and age-dependent hippocampal neuron sodium currents correlate with epilepsy severity in Dravet syndrome mice. Neurobiol. Dis. 2014, 65:1-11.
115. Nabbout R. A risk-benefit assessment of treatments for infantile spasms. Drug Saf. 2001, 24:813-828.
116. Nabbout R., Gennaro E., Dalla Bernardina B., Dulac O., Madia F., Bertini E., et al. Spectrum of SCN1A mutations in severe myoclonic epilepsy of infancy. Neurology 2003, 60:1961-1967.
117. Nagamitsu S., Matsuishi T., Yamashita Y., Shimizu T., Iwanaga R., Murakami Y., et al. Decreased cerebrospinal fluid levels of beta-endorphin and ACTH in children with infantile spasms. J. Neural Transm. 2001, 108:363-371.
118. Nakamura K., Kodera H., Akita T., Shiina M., Kato M., Hoshino H., et al. De Novo mutations in GNAO1, encoding a Galphao subunit of heterotrimeric G proteins, cause epileptic encephalopathy. Am. J. Hum. Genet. 2013, 93:496-505.
119. Nalin A., Facchinetti F., Galli V., Petraglia F., Storchi R., Genazzani A.R. Reduced ACTH content in cerebrospinal fluid of children affected by cryptogenic infantile spasms with hypsarrhythmia. Epilepsia 1985, 26:446-449.
120. Novara F., Rizzo A., Bedini G., Girgenti V., Esposito S., Pantaleoni C., et al. MEF2C deletions and mutations versus duplications: a clinical comparison. Eur. J. Med. Genet. 2013, 56:260-265.
121. Oakley J.C., Kalume F., Yu F.H., Scheuer T., Catterall W.A. Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3994-3999.
122. Oakley J.C., Cho A.R., Cheah C.S., Scheuer T., Catterall W.A. Synergistic GABA-enhancing therapy against seizures in a mouse model of Dravet syndrome. J. Pharmacol. Exp. Ther. 2013, 345:215-224.
123. Ogiwara I., Miyamoto H., Morita N., Atapour N., Mazaki E., Inoue I., et al. Nav1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J. Neurosci. 2007, 27:5903-5914.
124. Ogiwara I., Iwasato T., Miyamoto H., Iwata R., Yamagata T., Mazaki E., et al. Nav1.1 haploinsufficiency in excitatory neurons ameliorates seizure-associated sudden death in a mouse model of Dravet syndrome. Hum. Mol. Genet. 2013, 22:4784-4804.
125. Ohmori I., Ouchida M., Ohtsuka Y., Oka E., Shimizu K. Significant correlation of the SCN1A mutations and severe myoclonic epilepsy in infancy. Biochem. Biophys. Res. Commun. 2002, 295:17-23.
126. Ohmori I., Kawakami N., Liu S., Wang H., Miyazaki I., Asanuma M., et al. Methylphenidate improves learning impairments and hyperthermia-induced seizures caused by an Scn1a mutation. Epilepsia 2014, 55:1558-1567.
127. Olivetti P.R., Noebels J.L. Interneuron, interrupted: molecular pathogenesis of ARX mutations and X-linked infantile spasms. Curr. Opin. Neurobiol. 2012, 22:859-865.
128. Olivetti P.R., Maheshwari A., Noebels J.L. Neonatal estradiol stimulation prevents epilepsy in Arx model of X-linked infantile spasms syndrome. Sci. Transl. Med. 2014, 6:220ra212.
129. Ono T., Moshe S.L., Galanopoulou A.S. Carisbamate acutely suppresses spasms in a rat model of symptomatic infantile spasms. Epilepsia 2011, 52:1678-1684.
130. Orlova K.A., Crino P.B. The tuberous sclerosis complex. Ann. N. Y. Acad. Sci. 2010, 1184:87-105.
131. Orlova K.A., Parker W.E., Heuer G.G., Tsai V., Yoon J., Baybis M., et al. STRADalpha deficiency results in aberrant mTORC1 signaling during corticogenesis in humans and mice. J. Clin. Invest. 2010, 120:1591-1602.
132. Ostrach L.H., Crabtree J.W., Campbell B.G., Chow K.L. Effects of bicuculline-induced epileptiform activity on development of receptive field properties in striate cortex and lateral geniculate nucleus of the rabbit. Brain Res. 1984, 317:113-123.
133. Pan Y., Gerasimov M.R., Kvist T., Wellendorph P., Madsen K.K., Pera E., et al. (1S, 3S)-3-amino-4-difluoromethylenyl-1-cyclopentanoic acid (CPP-115), a potent gamma-aminobutyric acid aminotransferase inactivator for the treatment of cocaine addiction. J. Med. Chem. 2012, 55:357-366.
134. Parker W.E., Orlova K.A., Parker W.H., Birnbaum J.F., Krymskaya V.P., Goncharov D.A., et al. Rapamycin prevents seizures after depletion of STRADA in a rare neurodevelopmental disorder. Sci. Transl. Med. 2013, 5:182ra153.
135. Patino G.A., Claes L.R., Lopez-Santiago L.F., Slat E.A., Dondeti R.S., Chen C., et al. A functional null mutation of SCN1B in a patient with Dravet syndrome. J. Neurosci. 2009, 29:10764-10778.
136. Pellock J.M., Hrachovy R., Shinnar S., Baram T.Z., Bettis D., Dlugos D.J., et al. Infantile spasms: a U.S. consensus report. Epilepsia 2010, 51:2175-2189.
137. Pires M.E., Ilea A., Bourel E., Bellavoine V., Merdariu D., Berquin P., et al. Ketogenic diet for infantile spasms refractory to first-line treatments: an open prospective study. Epilepsy Res. 2013, 105:189-194.
138. Poole A.E., Brain P. Effects of adrenalectomy and treatments with ACTH and glucocorticoids on isolation-induced aggressive behavior in male albino mice. Prog. Brain Res. 1974, 41:465-472.
139. Price M.G., Yoo J.W., Burgess D.L., Deng F., Hrachovy R.A., Frost J.D., et al. A triplet repeat expansion genetic mouse model of infantile spasms syndrome, Arx(GCG)10+7, with interneuronopathy, spasms in infancy, persistent seizures, and adult cognitive and behavioral impairment. J. Neurosci. 2009, 29:8752-8763.
140. Pueschel S.M., Louis S., McKnight P. Seizure disorders in Down syndrome. Arch. Neurol. 1991, 48:318-320.
141. Raffo E., Coppola A., Ono T., Briggs S.W., Galanopoulou A.S. A pulse rapamycin therapy for infantile spasms and associated cognitive decline. Neurobiol. Dis. 2011, 43:322-329.
142. Reid C.A., Leaw B., Richards K.L., Richardson R., Wimmer V., Yu C., et al. Reduced dendritic arborization and hyperexcitability of pyramidal neurons in a Scn1b-based model of Dravet syndrome. Brain 2014, 137:1701-1715.
143. Riikonen R. Infantile spasms: some new theoretical aspects. Epilepsia 1983, 24:159-168.
144. Riikonen R. Recent advances in the pharmacotherapy of infantile spasms. CNS Drugs 2014, 28:279-290.
145. Romano C., Tine A., Fazio G., Rizzo R., Colognola R.M., Sorge G., et al. Seizures in patients with trisomy 21. Am. J. Med. Genet. Suppl. 1990, 7:298-300.
146. Saitsu H., Kato M., Okada I., Orii K.E., Higuchi T., Hoshino H., et al. STXBP1 mutations in early infantile epileptic encephalopathy with suppression-burst pattern. Epilepsia 2010, 51:2397-2405.
147. Sanmaneechai O., Sogawa Y., Silver W., Ballaban-Gil K., Moshe S.L., Shinnar S. Treatment outcomes of West syndrome in infants with Down syndrome. Pediatr. Neurol. 2013, 48:42-47.
148. Scala E., Ariani F., Mari F., Caselli R., Pescucci C., Longo I., et al. CDKL5/STK9 is mutated in Rett syndrome variant with infantile spasms. J. Med. Genet. 2005, 42:103-107.
149. Scantlebury M.H., Galanopoulou A.S., Chudomelova L., Raffo E., Betancourth D., Moshe S.L. A model of symptomatic infantile spasms syndrome. Neurobiol. Dis. 2010, 37:604-612.
150. Schneider M. Adolescence as a vulnerable period to alter rodent behavior. Cell Tissue Res. 2013, 354:99-106.
151. Schutte R.J., Schutte S.S., Algara J., Barragan E.V., Gilligan J., Staber C., et al. Knock-in model of Dravet Syndrome reveals a constitutive and conditional reduction in sodium current. J. Neurophysiol. 2014, 112:903-912.
152. Shatskikh T.N., Raghavendra M., Zhao Q., Cui Z., Holmes G.L. Electrical induction of spikes in the hippocampus impairs recognition capacity and spatial memory in rats. Epilepsy Behav. 2006, 9:549-556.
153. Shewmon D.A., Erwin R.J. Focal spike-induced cerebral dysfunction is related to the after-coming slow wave. Ann. Neurol. 1988, 23:131-137.
154. Shi X.Y., Zou L.P., Yang G., Ding Y.X. Prenatal stress exposure hypothesis for infantile spasms. Med. Hypotheses 2012, 78:735-737.
155. Silverman R.B. The 2011 E. B. Hershberg award for important discoveries in medicinally active substances: (1S,3S)-3-amino-4-difluoromethylenyl-1-cyclopentanoic acid (CPP-115), a GABA aminotransferase inactivator and new treatment for drug addiction and infantile spasms. J. Med. Chem. 2012, 55:567-575.
156. Silverstein F., Johnston M.V. Cerebrospinal fluid monoamine metabolites in patients with infantile spasms. Neurology 1984, 34:102-105.
157. Simonet J.C., Sunnen C.N., Wu J., Golden J.A., Marsh E.D. Conditional loss of Arx from the developing dorsal telencephalon results in behavioral phenotypes resembling mild human ARX mutations. Cereb. Cortex 2014, (Epub ahead of print).
158. Sprunger L.K., Escayg A., Tallaksen-Greene S., Albin R.L., Meisler M.H. Dystonia associated with mutation of the neuronal sodium channel Scn8a and identification of the modifier locus Scnm1 on mouse chromosome 3. Hum. Mol. Genet. 1999, 8:471-479.
159. Stafstrom C.E., Sasaki-Adams D.M. NMDA-induced seizures in developing rats cause long-term learning impairment and increased seizure susceptibility. Epilepsy Res. 2003, 53:129-137.
160. Stafstrom C.E., Moshe S.L., Swann J.W., Nehlig A., Jacobs M.P., Schwartzkroin P.A. Models of pediatric epilepsies: strategies and opportunities. Epilepsia 2006, 47:1407-1414.
161. Stromme P., Mangelsdorf M.E., Shaw M.A., Lower K.M., Lewis S.M., Bruyere H., et al. Mutations in the human ortholog of Aristaless cause X-linked mental retardation and epilepsy. Nat. Genet. 2002, 30:441-445.
162. Sturgill E.R., Aoki K., Lopez P.H., Colacurcio D., Vajn K., Lorenzini I., et al. Biosynthesis of the major brain gangliosides GD1a and GT1b. Glycobiology 2012, 22:1289-1301.
163. Sugawara T., Mazaki-Miyazaki E., Fukushima K., Shimomura J., Fujiwara T., Hamano S., et al. Frequent mutations of SCN1A in severe myoclonic epilepsy in infancy. Neurology 2002, 58:1122-1124.
164. Tang B., Dutt K., Papale L., Rusconi R., Shankar A., Hunter J., et al. A BAC transgenic mouse model reveals neuron subtype-specific effects of a generalized epilepsy with febrile seizures plus (GEFS+) mutation. Neurobiol. Dis. 2009, 35:91-102.
165. Tassinari C.A., Michelucci R., Forti A., Salvi F., Plasmati R., Rubboli G., et al. The electrical status epilepticus syndrome. Epilepsy Res. Suppl. 1992, 6:111-115.
166. Thiele E.A. Managing epilepsy in tuberous sclerosis complex. J. Child Neurol. 2004, 19:680-686.
167. Veeramah K.R., O'Brien J.E., Meisler M.H., Cheng X., Dib-Hajj S.D., Waxman S.G., et al. De novo pathogenic SCN8A mutation identified by whole-genome sequencing of a family quartet affected by infantile epileptic encephalopathy and SUDEP. Am. J. Hum. Genet. 2012, 90:502-510.
168. Velisek L., Mares P. Age-dependent anticonvulsant action of clonazepam in the N-methyl-D-aspartate model of seizures. Pharmacol. Biochem. Behav. 1995, 52:291-296.
169. Velisek L., Jehle K., Asche S., Veliskova J. Model of infantile spasms induced by N-methyl-D-aspartic acid in prenatally impaired brain. Ann. Neurol. 2007, 61:109-119.
170. Wagnon J.L., Korn M.J., Parent R., Tarpey T.A., Jones J.M., Hammer M.F., et al. Convulsive seizures and SUDEP in a mouse model of SCN8A epileptic encephalopathy. Hum. Mol. Genet. 2015, 24:506-515.
171. Wang I.T., Allen M., Goffin D., Zhu X., Fairless A.H., Brodkin E.S., et al. Loss of CDKL5 disrupts kinome profile and event-related potentials leading to autistic-like phenotypes in mice. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:21516-21521.
172. Wang J., Wang J., Zhang Y., Yang G., Zhou W.J., Shang A.J., et al. Proteomic analysis of adrenocorticotropic hormone treatment of an infantile spasm model induced by N-methyl-D-aspartic acid and prenatal stress. PLoS One 2012, 7:e45347.
173. Wang Y.J., Zhang Y., Liang X.H., Yang G., Zou L.P. Effects of adrenal dysfunction and high-dose adrenocorticotropic hormone on NMDA-induced spasm seizures in young Wistar rats. Epilepsy Res. 2012, 100:125-131.
174. Watanabe H., Nagata E., Kosakai A., Nakamura M., Yokoyama M., Tanaka K., et al. Disruption of the epilepsy KCNQ2 gene results in neural hyperexcitability. J. Neurochem. 2000, 75:28-33.
175. Weaving L.S., Christodoulou J., Williamson S.L., Friend K.L., McKenzie O.L., Archer H., et al. Mutations of CDKL5 cause a severe neurodevelopmental disorder with infantile spasms and mental retardation. Am. J. Hum. Genet. 2004, 75:1079-1093.
176. West W.J. On a peculiar form of infantile convulsions. Lancet Neurol. 1841, 1:724-725.
177. Wiegand G., May T.W., Ostertag P., Boor R., Stephani U., Franz D.N. Everolimus in tuberous sclerosis patients with intractable epilepsy: a treatment option?. Eur. J. Paediatr. Neurol. 2013, 17:631-638.
178. Willig R.P., Lagenstein I., Iffland E. Circadian rhythm of cortisol under ACTH and dexamethasone therapy of convulsions in early childhood (BNS- and Lennox-syndrome) (author's transl). Monatsschr. Kinderheilkd. 1978, 126:191-197.
179. Yamamoto H. Studies on CSF tryptophan metabolism in infantile spasms. Pediatr. Neurol. 1991, 7:411-414.
180. Yang Y., Beyer B.J., Otto J.F., O'Brien T.P., Letts V.A., White H.S., et al. Spontaneous deletion of epilepsy gene orthologs in a mutant mouse with a low electroconvulsive threshold. Hum. Mol. Genet. 2003, 12:975-984.
181. Yu F.H., Mantegazza M., Westenbroek R.E., Robbins C.A., Kalume F., Burton K.A., et al. Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat. Neurosci. 2006, 9:1142-1149.
182. Yum M.S., Chachua T., Veliskova J., Velisek L. Prenatal stress promotes development of spasms in infant rats. Epilepsia 2012, 53:e46-e49.
183. Yum M.S., Lee M., Ko T.S., Velisek L. A potential effect of ganaxolone in an animal model of infantile spasms. Epilepsy Res. 2014, 108:1492-1500.
184. Zeng L.H., Xu L., Gutmann D.H., Wong M. Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Ann. Neurol. 2008, 63:444-453.
185. Zhou J.L., Lenck-Santini P.P., Zhao Q., Holmes G.L. Effect of interictal spikes on single-cell firing patterns in the hippocampus. Epilepsia 2007, 48:720-731.