Characterization of a de novo SCN8A mutation in a patient with epileptic encephalopathy

Epilepsy Research

Volumn 108, Issue 9, 2014, Pages 1511-1518

  de Kovel, Carolien G F ^a   Meisler, Miriam H ^b   Brilstra, Eva H ^a   van Berkestijn, Frederique M C ^a   Slot, Ruben van 't ^a   van Lieshout, Stef ^a   Nijman, Isaac J ^a   O'Brien, Janelle E ^b   Hammer, Michael F ^e   Estacion, Mark ^c,d   Waxman, Stephen G ^c,d   Dib Hajj, Sulayman D ^c,d   Koeleman, Bobby P C ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

Epileptic encephalopathy; Exome sequencing; Nav1.6; Patch clamp; SCN8A

Indexed keywords

COMPLEMENTARY DNA; ETIRACETAM; MAGNESIUM; METHYLPREDNISOLONE; MIDAZOLAM; MUTANT PROTEIN; NITRAZEPAM; PHENOBARBITAL; PHENYTOIN; PROPOFOL; PYRIDOXAL 5 PHOSPHATE; SODIUM CHANNEL NAV1.6; THIOPENTAL; TOPIRAMATE; VIGABATRIN; ARGININE; GLYCINE; SCN8A PROTEIN, HUMAN;

ARTICLE; BRAIN ATROPHY; BRAIN DISEASE; CONTROLLED STUDY; EPILEPTIC ENCEPHALOPATHY; EXOME; GENE; GENE SEQUENCE; HEK293 CELL LINE; HUMAN; HUMAN CELL; INTERNEURON; MISSENSE MUTATION; OPEN READING FRAME; PATCH CLAMP TECHNIQUE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN STABILITY; SCN8A GENE; SODIUM CURRENT; TEMPERATURE SENSITIVITY; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING; WILD TYPE; CASE REPORT; COMPLICATION; EPILEPSY; FEMALE; GENETIC TRANSFECTION; GENETICS; MEMBRANE POTENTIAL; MICROCEPHALY; MUTATION; PRESCHOOL CHILD; TEMPERATURE;

ARGININE; CHILD, PRESCHOOL; EPILEPSY; FEMALE; GLYCINE; HEK293 CELLS; HUMANS; MEMBRANE POTENTIALS; MICROCEPHALY; MUTATION; NAV1.6 VOLTAGE-GATED SODIUM CHANNEL; PATCH-CLAMP TECHNIQUES; TEMPERATURE; TRANSFECTION;

EID: 84908010182     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2014.08.020     Document Type: Article

References (38)

1. 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., Malone S., Wallace G., Stanley T., Bye A.M., Bleasel A., Howell K.B., Kivity S., Mackay M.T., Rodriguez-Casero V., Webster R., Korczyn A., Afawi Z., Zelnick N., Lerman-Sagie T., Lev D., Moller R.S., Gill D., Andrade D.M., Freeman J.L., Sadleir L.G., Shendure J., Berkovic S.F., Scheffer I.E., Mefford H.C. Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet. 2013, 45:825-830.
2. Cestele S., Schiavon E., Rusconi R., Franceschetti S., Mantegazza M. Nonfunctional NaV1.1 familial hemiplegic migraine mutant transformed into gain of function by partial rescue of folding defects. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17546-17551.
3. Cheah C.S., Yu F.H., Westenbroek R.E., Kalume F.K., Oakley J.C., Potter G.B., Rubenstein J.L., Catterall W.A. 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.
4. Claes L.R., Deprez L., Suls A., Baets J., Smets K., Van Dyck T., Deconinck T., Jordanova A., De Jonghe P. The SCN1A variant database: a novel research and diagnostic tool. Hum. Mutat. 2009, 30:E904-E920.
5. Cummins T.R., Howe J.R., Waxman S.G. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J. Neurosci. 1998, 18:9607-9619.
6. Dutton S.B., Makinson C.D., Papale L.A., Shankar A., Balakrishnan B., Nakazawa K., Escayg A. Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiol. Dis. 2012, 49C:211-220.
7. Epi4K-Consortium, Epilepsy Phenome/Genome P., 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., Heinzen E.L., Hitomi Y., Howell K.B., Johnson M.R., Kuzniecky R., Lowenstein D.H., Lu Y.F., Madou M.R., Marson A.G., Mefford H.C., Esmaeeli Nieh S., O'Brien T.J., Ottman R., Petrovski S., Poduri A., Ruzzo E.K., Scheffer I.E., Sherr E.H., Yuskaitis C.J., Abou-Khalil B., Alldredge B.K., Bautista J.F., Berkovic S.F., Boro A., Cascino G.D., Consalvo D., Crumrine P., Devinsky O., Dlugos D., Epstein M.P., Fiol M., Fountain N.B., French J., Friedman D., Geller E.B., Glauser T., Glynn S., Haut S.R., Hayward J., Helmers S.L., Joshi S., Kanner A., Kirsch H.E., Knowlton R.C., Kossoff E.H., Kuperman R., Kuzniecky R., Lowenstein D.H., McGuire S.M., Motika P.V., Novotny E.J., Ottman R., Paolicchi J.M., Parent J.M., Park K., Poduri A., Scheffer I.E., Shellhaas R.A., Sherr E.H., Shih J.J., Singh R., Sirven J., Smith M.C., Sullivan J., Lin Thio L., Venkat A., Vining E.P., Von Allmen G.K., Weisenberg J.L., Widdess-Walsh P., Winawer M.R. De novo mutations in epileptic encephalopathies. Nature 2013, 501:217-221.
8. Estacion M., O'Brien J.E., Conravey A., Hammer M.F., Waxman S.G., Dib-Hajj S.D., Meisler M.H. A novel de novo mutation of SCN8A (Nav1.6) with enhanced channel activation in a child with epileptic encephalopathy. Neurobiol Dis. 2014, 45:117-123.
9. Estacion M., Waxman S.G. The response of Na(V)1.3 sodium channels to ramp stimuli: multiple components and mechanisms. J. Neurophysiol. 2013, 109:306-314.
10. Hu W., Tian C., Li T., Yang M., Hou H., Shu Y. Distinct contributions of Na(v)1.6 and Na(v)1.2 in action potential initiation and backpropagation. Nat. Neurosci. 2009, 12:996-1002.
11. Jones J.M., Meisler M.H. Modeling human epilepsy by TALEN targeting of mouse sodium channel Scn8a. Genesis 2014, 52:141-148.
12. Lenk G.M., Ferguson C.J., Chow C.Y., Jin N., Jones J.M., Grant A.E., Zolov S.N., Winters J.J., Giger R.J., Dowling J.J., Weisman L.S., Meisler M.H. Pathogenic mechanism of the FIG4 mutation responsible for Charcot-Marie--Tooth disease CMT4J. PLoS Genet. 2011, 7:e1002104.
13. Liu Y., Lopez-Santiago L.F., Yuan Y., Jones J.M., Zhang H., O'Malley H.A., Patino G.A., O'Brien J.E., Rusconi R., Gupta A., Thompson R.C., Natowicz M.R., Meisler M.H., Isom L.L., Parent J.M. Dravet syndrome patient-derived neurons suggest a novel epilepsy mechanism. Ann. Neurol. 2013, 74:128-139.
14. Lorincz A., Nusser Z. Cell-type-dependent molecular composition of the axon initial segment. J. Neurosci. 2008, 28:14329-14340.
15. Lorincz A., Nusser Z. Molecular identity of dendritic voltage-gated sodium channels. Science 2010, 328:906-909.
16. Meisler M.H., O'Brien J.E., Sharkey L.M. Sodium channel gene family: epilepsy mutations, gene interactions and modifier effects. J. Physiol. 2010, 588:1841-1848.
17. Meisler M.H., Kearney J.A. Sodium channel mutations in epilepsy and other neurological disorders. J. Clin. Invest. 2005, 115:2010-2017.
18. Mulley J.C., Scheffer I.E., Petrou S., Dibbens L.M., Berkovic S.F., Harkin L.A. SCN1A mutations and epilepsy. Hum. Mutat. 2005, 25:535-542.
19. Nijman I.J., Mokry M., van Boxtel R., Toonen P., de Bruijn E., Cuppen E. Mutation discovery by targeted genomic enrichment of multiplexed barcoded samples. Nat. Methods 2010, 7:913-915.
20. O'Brien J.E., Meisler M.H. Sodium channel (Na1.6): properties and mutations in epileptic encephalopathy and intellectual disability. Front. Genet. 2013, 4:213.
21. Ogiwara I., Ito K., Sawaishi Y., Osaka H., Mazaki E., Inoue I., Montal M., Hashikawa T., Shike T., Fujiwara T., Inoue Y., Kaneda M., Yamakawa K. De novo mutations of voltage-gated sodium channel alphaII gene SCN2A in intractable epilepsies. Neurology 2009, 73:1046-1053.
22. Ogiwara I., Iwasato T., Miyamoto H., Iwata R., Yamagata T., Mazaki E., Yanagawa Y., Tamamaki N., Hensch T.K., Itohara S., Yamakawa K. 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.
23. Oliva M., Berkovic S.F., Petrou S. Sodium channels and the neurobiology of epilepsy. Epilepsia 2012, 53:1849-1859.
24. Oliva M.K., McGarr T.C., Beyer B.J., Gazina E., Kaplan D.I., Cordeiro L., Thomas E., Dib-Hajj S.D., Waxman S.G., Frankel W.N., Petrou S. Physiological and genetic analysis of multiple sodium channel variants in a model of genetic absence epilepsy. Neurobiol. Dis 2014, 67:180-190.
25. Papale L.A., Beyer B., Jones J.M., Sharkey L.M., Tufik S., Epstein M., Letts V.A., Meisler M.H., Frankel W.N., Escayg A. Heterozygous mutations of the voltage-gated sodium channel SCN8A are associated with spike-wave discharges and absence epilepsy in mice. Hum. Mol. Genet. 2009, 18:1633-1641.
26. Plummer N.W., Galt J., Jones J.M., Burgess D.L., Sprunger L.K., Kohrman D.C., Meisler M.H. Exon organization, coding sequence, physical mapping, and polymorphic intragenic markers for the human neuronal sodium channel gene SCN8A. Genomics 1998, 54:287-296.
27. Rauch A., Wieczorek D., Graf E., Wieland T., Endele S., Schwarzmayr T., Albrecht B., Bartholdi D., Beygo J., Di Donato N., Dufke A., Cremer K., Hempel M., Horn D., Hoyer J., Joset P., Ropke A., Moog U., Riess A., Thiel C.T., Tzschach A., Wiesener A., Wohlleber E., Zweier C., Ekici A.B., Zink A.M., Rump A., Meisinger C., Grallert H., Sticht H., Schenck A., Engels H., Rappold G., Schrock E., Wieacker P., Riess O., Meitinger T., Reis A., Strom T.M. Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study. Lancet 2012, 380:1674-1682.
28. Royeck M., Horstmann M.T., Remy S., Reitze M., Yaari Y., Beck H. Role of axonal NaV1.6 sodium channels in action potential initiation of CA1 pyramidal neurons. J. Neurophysiol. 2008, 100:2361-2380.
29. Rush A.M., Dib-Hajj S.D., Waxman S.G. Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J. Physiol. 2005, 564:803-815.
30. Scheffer I.E., Zhang Y.H., Jansen F.E., Dibbens L. Dravet syndrome or genetic (generalized) epilepsy with febrile seizures plus?. Brain Dev. 2009, 31:394-400.
31. v1.6 disrupts intracellular trafficking. J. Neurosci. 2009, 29:2733-2741.
32. Shi X., Yasumoto S., Kurahashi H., Nakagawa E., Fukasawa T., Uchiya S., Hirose S. Clinical spectrum of SCN2A mutations. Brain Dev. 2012, 34:541-545.
33. Sun W., Wagnon J.L., Mahaffey C.L., Briese M., Ule J., Frankel W.N. Aberrant sodium channel activity in the complex seizure disorder of Celf4 mutant mice. J. Physiol. 2013, 591:241-255.
34. Trudeau M.M., Dalton J.C., Day J.W., Ranum L.P., Meisler M.H. Heterozygosity for a protein truncation mutation of sodium channel SCN8A in a patient with cerebellar atrophy, ataxia, and mental retardation. J. Med. Genet. 2006, 43:527-530.
35. Vaher U., Noukas M., Nikopensius T., Kals M., Annilo T., Nelis M., Ounap K., Reimand T., Talvik I., Ilves P., Piirsoo A., Seppet E., Metspalu A., Talvik T. 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. 2013, Epub ahead of print.
36. Van Wart A., Matthews G. Impaired firing and cell-specific compensation in neurons lacking Nav1.6 sodium channels. J. Neurosci. 2006, 26:7172-7180.
37. 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., Erickson R.P., Hammer M.F. 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.
38. Vega A.V., Henry D.L., Matthews G. Reduced expression of Na(v)1.6 sodium channels and compensation by Na(v)1.2 channels in mice heterozygous for a null mutation in Scn8a. Neurosci. Lett. 2008, 442:69-73.