Convulsive seizures and SUDEP in a mouse model of SCN8A epileptic encephalopathy

Human Molecular Genetics

Volumn 24, Issue 2, 2015, Pages 506-515

  Wagnon, Jacy L ^a   Korn, Matthew J ^a   Parent, Rachel ^b   Tarpey, Taylor A ^b   Jones, Julie M ^a   Hammer, Michael F ^c   Murphy, Geoffrey G ^b,d   Parent, Jack M ^a,e   Meisler, Miriam H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^e VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; SODIUM CHANNEL NAV1.6; VOLTAGE GATED SODIUM CHANNEL; SCN8A PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTIC ENCEPHALOPATHY; GAIN OF FUNCTION MUTATION; GENE; GENE MUTATION; GENETIC TRANSFECTION; HETEROZYGOSITY; HETEROZYGOTE; HOMOZYGOSITY; HYPERACTIVITY; IN VIVO STUDY; MOTOR COORDINATION; MOUSE; MYOCLONUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SCN8A GENE; SEIZURE; SOCIAL DISCRIMINATION; SODIUM CURRENT; SUDDEN DEATH; ANIMAL; BEHAVIOR; BRUGADA SYNDROME; DISEASE MODEL; FEMALE; GENE TARGETING; GENETICS; HUMAN; MALE; METABOLISM; MISSENSE MUTATION; PSYCHOLOGY;

MUS;

ANIMALS; BEHAVIOR; BRUGADA SYNDROME; DISEASE MODELS, ANIMAL; EPILEPSY; FEMALE; GENE KNOCK-IN TECHNIQUES; HUMANS; MALE; MICE; MUTATION, MISSENSE; NAV1.6 VOLTAGE-GATED SODIUM CHANNEL; SEIZURES;

EID: 84922475507     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu470     Document Type: Article

References (46)

1. Berg, A.T., Berkovic, S.F., Brodie, M.J., Buchhalter, J., Cross, J.H., van Emde Boas, W., Engel, J., French, J., Glauser, T.A., Mathern, G.W. et al. (2010) Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia, 51, 676-685.
2. Carvill, G.L., Heavin, S.B., Yendle, S.C., McMahon, J.M., O'Roak, B.J., Cook, J., Khan, A., Dorschner, M.O., Weaver, M., Calvert, S. et al. (2013) Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet., 45, 825-830.
3. Epi4K Consortium; Epilepsy Phenome/Genome Project; Allen, A.S., Berkovic, S.F., Cossette, P., Delanty, N., Dlugos, D., Eichler, E.E., Epstein, M.P., Glauser, T., Goldstein, D.B., Han, Y. et al. (2013) De novo mutations in epileptic encephalopathies. Nature, 501, 217-221.
4. Kodera, H., Kato, M., Nord, A.S., Walsh, T., Lee, M., Yamanaka, G., Tohyama, J., Nakamura, K., Nakagawa, E., Ikeda, T. et al. (2013) Targeted capture and sequencing for detection of mutations causing early onset epileptic encephalopathy. Epilepsia, 54, 1262-1269.
5. Veeramah, K.R., Johnstone, L., Karafet, T.M., Wolf, D., Sprissler, R., Salogiannis, J., Barth-Maron, A., Greenberg, M.E., Stuhlmann, T., Weinert, S. et al. (2013) Exome sequencing reveals new causal mutations in children with epileptic encephalopathies. Epilepsia, 54, 1270-1281.
6. Mastrangelo, M. and Leuzzi, V. (2012) Genes of early-onset epileptic encephalopathies: from genotype to phenotype. Pediatr. Neurol., 46, 24-31.
7. Nicita, F., De Liso, P., Danti, F.R., Papetti, L., Ursitti, F., Castronovo, A., Allemand, F., Gennaro, E., Zara, F., Striano, P. et al. (2012) The genetics of monogenic idiopathic epilepsies and epileptic encephalopathies. Seizure, 21, 3-11.
8. Meisler, M.H., O'Brien, J.E. and Sharkey, L.M. (2010) Sodiumchannel gene family: epilepsy mutations, gene interactions and modifier effects. J. Physiol., 588, 1841-1848.
9. Veeramah, K.R., O'Brien, J.E., Meisler, M.H., Cheng, X., Dib-Hajj, S.D., Waxman, S.G., Talwar, D., Girirajan, S., Eichler, E.E., Restifo, L.L. et al. (2012) 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., 90, 502-510.
10. Dyment, D.A., Tetreault, M., Beaulieu, C.L., Hartley, T., Ferreira, P., Warman Chardon, J., Marcadier, J., Sawyer, S.L., Mosca, S.J., Micheil Innes, A. et al. (2014) Whole-exome sequencing broadens the phenotypic spectrum of rare pediatric epilepsy: a retrospective study. Clin. Genet., doi: 10.1111/cge.12464.
11. Estacion, M., O'Brien, J.E., Conravey, A., Hammer, M.F., Waxman, S.G., Dib-Hajj, S.D. and Meisler, M.H. (2014) A novel de novo mutation of SCN8A (Na1.6) with enhanced channel activation in a child with epileptic encephalopathy. Neurobiol. Dis., 69C, 117-123.
12. O'Brien, J.E. and Meisler, M.H. (2013) Sodium channel SCN8A (Nav1.6): properties and de novo mutations in epileptic encephalopathy and intellectual disability. Front. Genet., 4, 213.
13. Ohba, C., Kato, M., Takahashi, S., Lerman-Sagie, T., Lev, D., Terashima, H., Kubota, M., Kawawaki, H., Matsufuji, M., Kojima, Y. et al. (2014) Early onset epileptic encephalopathy caused by de novo SCN8A mutations. Epilepsia, 55, 994-1000.
14. Rauch, A., Wieczorek, D., Graf, E., Wieland, T., Endele, S., Schwarzmayr, T., Albrecht, B., Bartholdi, D., Beygo, J., Di Donato, N. et al. (2012) Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exomesequencing study. Lancet, 380, 1674-1682.
15. Vaher, U., Noukas, M., Nikopensius, T., Kals, M., Annilo, T., Nelis, M., Ounap, K., Reimand, T., Talvik, I., Ilves, P. et al. (2013) De Novo SCN8A Mutation identified by whole-exome sequencing in a boy with neonatal epileptic encephalopathy, multiple congenital anomalies, and movement disorders. J. Child. Neurol., doi:10.1177/0883073813511300.
16. Boiko, T., Rasband, M.N., Levinson, S.R., Caldwell, J.H., Mandel, G., Trimmer, J.S. and Matthews, G. (2001) Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron, 30, 91-104.
17. Boiko, T., Van Wart, A., Caldwell, J.H., Levinson, S.R., Trimmer, J.S. and Matthews, G. (2003) Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J. Neurosci., 23, 2306-2313.
18. Caldwell, J.H., Schaller, K.L., Lasher, R.S., Peles, E. and Levinson, S.R. (2000) Sodium channel Na(v)1.6 is localized at nodes of ranvier, dendrites, and synapses. Proc. Natl. Acad. Sci. USA, 97, 5616-5620.
19. Krzemien, D.M., Schaller, K.L., Levinson, S.R. and Caldwell, J.H. (2000) Immunolocalization of sodium channel isoform NaCh6 in the nervous system. J. Comp. Neurol., 420, 70-83.
20. Hu, W., Tian, C., Li, T., Yang, M., Hou, H. and Shu, Y. (2009) Distinct contributions of Na(v)1.6 and Na(v)1.2 in action potential initiation and backpropagation. Nat. Neurosci., 12, 996-1002.
21. Lorincz, A. and Nusser, Z. (2008) Cell-type-dependent molecular composition of the axon initial segment. J. Neurosci., 28, 14329-14340.
22. Van Wart, A., Trimmer, J.S. and Matthews, G. (2007) Polarized distribution of ion channels within microdomains of the axon initial segment. J. Comp. Neurol., 500, 339-352.
23. Jones, J.M. and Meisler, M.H. (2014) Modeling human epilepsy by TALEN targeting of mouse sodium channel Scn8a. Genesis, 52, 141-148.
24. Burgess, D.L., Kohrman, D.C., Galt, J., Plummer, N.W., Jones, J.M., Spear, B. and Meisler, M.H. (1995) Mutation of a new sodium channel gene, Scn8a, in the mouse mutant 'motor endplate disease'. Nat. Genet., 10, 461-465.
25. Sharkey, L.M., Cheng, X., Drews, V., Buchner, D.A., Jones, J.M., Justice, M.J., Waxman, S.G., Dib-Hajj, S.D. and Meisler, M.H. (2009) The ataxia3 mutation in the N-terminal cytoplasmic domain of sodium channel Na(v)1.6 disrupts intracellular trafficking. J. Neurosci., 29, 2733-2741.
26. Ryvlin, P., Nashef, L., Lhatoo, S.D., Bateman, L.M., Bird, J., Bleasel, A., Boon, P., Crespel, A., Dworetzky, B.A., Hogenhaven, H. et al. (2013) Incidence and mechanisms of cardiorespiratory arrests in epilepsy monitoring units (MORTEMUS): a retrospective study. Lancet Neurol., 12, 966-977.
27. McKinney, B.C., Chow, C.Y., Meisler, M.H. and Murphy, G.G. (2008) Exaggerated emotional behavior in mice heterozygous null for the sodium channel Scn8a (Nav1.6). Genes Brain Behav., 7, 629-638.
28. Liao, Y., Deprez, L., Maljevic, S., Pitsch, J., Claes, L., Hristova, D., Jordanova, A., Ala-Mello, S., Bellan-Koch, A., Blazevic, D. et al. (2010) Molecular correlates of age-dependent seizures in an inherited neonatal-infantile epilepsy. Brain, 133, 1403-1414.
29. Osorio, N., Cathala, L., Meisler, M.H., Crest, M., Magistretti, J. and Delmas, P. (2010) Persistent Nav1.6 current at axon initial segments tunes spike timing of cerebellar granule cells. J. Physiol., 588, 651-670.
30. Kohrman, D.C., Harris, J.B. and Meisler, M.H. (1996) Mutation detection in the med and medJ alleles of the sodium channel Scn8a. Unusual splicing due to a minor class AT-AC intron. J. Biol. Chem., 271, 17576-17581.
31. Bender, A.C., Natola, H., Ndong, C., Holmes, G.L., Scott, R.C. and Lenck-Santini, P.P. (2013) Focal Scn1a knockdown induces cognitive impairment without seizures. Neurobiol. Dis., 54, 297-307.
32. Han, S., Tai, C., Westenbroek, R.E., Yu, F.H., Cheah, C.S., Potter, G.B., Rubenstein, J.L., Scheuer, T., de la Iglesia, H.O. and Catterall, W.A. (2012) Autistic-like behaviour in Scn1a+/2 mice and rescue by enhanced GABA-mediated neurotransmission. Nature, 489, 385-390.
33. Trudeau, M.M., Dalton, J.C., Day, J.W., Ranum, L.P. and Meisler, M.H. (2006) Heterozygosity for a protein truncation mutation of sodium channel SCN8A in a patient with cerebellar atrophy, ataxia, and mental retardation. J. Med. Genet., 43, 527-530.
34. Kearney, J.A., Buchner, D.A., DeHaan, G., Adamska, M., Levin, S.I., Furay, A.R., Albin, R.L., Jones, J.M., Montal, M., Stevens, M.J. et al. (2002) Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a (Na(v)1.6). Hum. Mol. Genet., 11, 2765-2775.
35. Sprunger, L.K., Escayg, A., Tallaksen-Greene, S., Albin, R.L. and Meisler, M.H. (1999) Dystonia associated with mutation of the neuronal sodium channel Scn8a and identification of the modifier locus Scnm1 on mouse chromosome 3. Hum. Mol. Genet., 8, 471-479.
36. Kohrman, D.C., Smith, M.R., Goldin, A.L., Harris, J. and Meisler, M.H. (1996) A missense mutation in the sodium channel Scn8a is responsible for cerebellar ataxia in the mouse mutant jolting. J. Neurosci., 16, 5993-5999.
37. Hawkins, N.A., Martin, M.S., Frankel, W.N., Kearney, J.A. and Escayg, A. (2011) Neuronal voltage-gated ion channels are genetic modifiers of generalized epilepsy with febrile seizures plus. Neurobiol. Dis., 41, 655-660.
38. Martin, M.S., Tang, B., Papale, L.A., Yu, F.H., Catterall, W.A. and Escayg, A. (2007) The voltage-gated sodium channel Scn8a is a genetic modifier of severe myoclonic epilepsy of infancy. Hum. Mol. Genet., 16, 2892-2899.
39. Sun, W., Wagnon, J.L., Mahaffey, C.L., Briese, M., Ule, J. and Frankel, W.N. (2013) Aberrant sodium channel activity in the complex seizure disorder of Celf4 mutant mice. J. Physiol., 591, 241-255.
40. Papale, L.A., Beyer, B., Jones, J.M., Sharkey, L.M., Tufik, S., Epstein, M., Letts, V.A., Meisler, M.H., Frankel, W.N. and Escayg, A. (2009) Heterozygous mutations of the voltage-gated sodium channel SCN8A are associated with spike-wave discharges and absence epilepsy in mice. Hum. Mol. Genet., 18, 1633-1641.
41. O'Brien, J.E., Sharkey, L.M., Vallianatos, C.N., Han, C., Blossom, J.C., Yu, T., Waxman, S.G., Dib-Hajj, S.D. and Meisler, M.H. (2012) Interaction of voltage-gated sodium channel Nav1.6 (SCN8A) with microtubuleassociated protein Map1b. J. Biol. Chem., 287, 18459-18466.
42. Kehrl, J.M., Sahaya, K., Dalton, H.M., Charbeneau, R.A., Kohut, K.T., Gilbert, K., Pelz, M.C., Parent, J. and Neubig, R.R. (2014) Gain-of-function mutation in Gnao1: a murine model of epileptiform encephalopathy (EIEE17)? Mamm. Genome, 25, 202-210.
43. Lee, C.H., Javed, D., Althaus, A.L., Parent, J.M. and Umemori, H. (2012) Neurogenesis is enhanced and mossy fiber sprouting arises in FGF7-deficient mice during development. Mol. Cell. Neurosci., 51, 61-67.
44. Nadler, J.J., Moy, S.S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N.B., Barbaro, R.P., Piven, J., Magnuson, T.R. et al. (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav., 3, 303-314.
45. de Kovel, C.G.F., Meisler, M., Brilstra, E.H., van Berkestijn, F.M., van t'Slot, R., van Lieshout, S., Nijman, I.J., O'Brien, J.E., Hammer, M.F., Estacion, M. et al. (2014) Characterization of a de novo SCN8 Amutation in a patient with epileptic encephalopathy. Epilepsy Res., doi:10.1016/j.eplepsyres.2014.08.020.
46. Larsen, J., Carvill, G.L., Gardella, E., Kluger, G., Schmiedel, G., Barisic, N., Depienne, C., Brilstra, E., Mang, Y., Nielsen, J.E.K. et al. (2014) The phenotypic spectrum of SCN8A encephalopathy. Neurology, in press.