Sodium channel gene family: Epilepsy mutations, gene interactions and modifier effects

Journal of Physiology

Volumn 588, Issue 11, 2010, Pages 1841-1848

  Meisler, Miriam H ^a   O'Brien, Janelle E ^a   Sharkey, Lisa M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL;

ACTION POTENTIAL; AMINO ACID SUBSTITUTION; CENTRAL NERVOUS SYSTEM; CHANNELOPATHY; DRAVET SYNDROME; EPILEPSY; GENE; GENE INTERACTION; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; KCNQ2 GENE; MULTIGENE FAMILY; MYOCLONUS EPILEPSY; PERIPHERAL NERVOUS SYSTEM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; SCN1A GENE; SCN2A GENE; SCN3A GENE; SCN8A GENE; SCN9A GENE;

ANIMALS; CHANNELOPATHIES; CHROMOSOMES; EPILEPSY; EPITHELIAL SODIUM CHANNEL; HUMANS; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM CHANNELS;

EID: 77954514571     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.188482     Document Type: Review

References (59)

1. Audenaert D, De Jonghe P. A deletion in SCN1B is associated with febrile seizures and early-onset absence epilepsy. Neurology 2003, 61:854-856.
2. Bergren SK, Chen S, Galecki A, Kearney JA. Genetic modifiers affecting severity of epilepsy caused by mutation of sodium channel Scn2a. Mamm Genome 2005, 16:683-690.
3. Bergren SK, Rutter ED, Kearney JA. Fine mapping of an epilepsy modifier gene on mouse Chromosome 19. Mamm Genome 2009, 20:359-366.
4. Blumenfeld H, Lampert A, Klein JP, Mission J, Chen MC, Rivera M, Dib-Hajj S, Brennan AR, Hains BC, Waxman SG. Role of hippocampal sodium channel Nav1.6 in kindling epileptogenesis. Epilepsia 2009, 50:44-55.
5. Brackenbury WJ, Djamgoz MB, Isom LL. An emerging role for voltage-gated Na+ channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers. Neuroscientist 2008, 14:571-583.
6. Brackenbury WJ, Calhoun JD, Chen C, Miyazaki H, Nukina N, Oyama F, Ranscht B, Isom LL. Functional reciprocity between Na+ channel Nav1.6 and β1 subunits in the coordinated regulation of excitability and neurite outgrowth. Proc Natl Acad Sci U S A 2010, 107:2283-2288.
7. Burgess DL. Neonatal epilepsy syndromes and GEFS+: mechanistic considerations. Epilepsia 2005, 46(Suppl 10):51-58.
8. Chen C, Dickendesher TL, Oyama F, Miyazaki H, Nukina N, Isom LL. Floxed allele for conditional inactivation of the voltage-gated sodium channel beta1 subunit Scn1b. Genesis 2007, 45:547-553.
9. 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.
10. Claes LR, 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:E904-920.
11. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, Saphier G, Leibel R, Goland R, Wichterle H, Henderson CE, Eggan K. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
12. Dib-Hajj SD, Binshtok AM, Cummins TR, Jarvis MF, Samad T, Zimmermann K. Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res Rev 2009, 60:65-83.
13. Ebert AD, Yu J, Rose FF, Mattis VB, Lorson CL, Thomson JA, Svendsen CN. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457:277-280.
14. Escayg A, MacDonald BT, Meisler MH, Baulac S, Huberfeld G, An-Gourfinkel I, Brice A, LeGuern E, Moulard B, Chaigne D, Buresi C, Malafosse A. Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat Genet 2000, 24:343-345.
15. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG. Sodium channel α-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res 1997, 45:71-82.
16. Glasscock E, Qian J, Yoo JW, Noebels JL. Masking epilepsy by combining two epilepsy genes. Nat Neurosci 2007, 10:1554-1558.
17. Heinzen EL, Yoon W, Tate SK, Sen A, Wood NW, Sisodiya SM, Goldstein DB. Nova2 interacts with a cis-acting polymorphism to influence the proportions of drug-responsive splice variants of SCN1A. Am J Hum Genet 2007, 80:876-883.
18. Holland KD, Kearney JA, Glauser TA, Buck G, Keddache M, Blankston JR, Glaaser IW, Kass RS, Meisler MH. Mutation of sodium channel SCN3A in a patient with cryptogenic pediatric partial epilepsy. Neurosci Lett 2008, 433:65-70.
19. Isom LL, De Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, Walsh K, Goldin AL, Catterall WA. Primary structure and functional expression of the β1 subunit of the rat brain sodium channel. Science 1992, 256:839-842.
20. Isom LL, Scheuer T, Brownstein AB, Ragsdale DS, Murphy BJ, Catterall WA. Functional co-expression of the β1 and type IIA α subunits of sodium channels in a mammalian cell line. J Biol Chem 1995, 270:3306-3312.
21. Kalume F, Yu FH, Westenbroek RE, Scheuer T, Catterall WA. 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.
22. Kamiya K, Kaneda M, Sugawara T, Mazaki E, Okamura N, Montal M, Makita N, Tanaka M, Fukushima K, Fujiwara T, Inoue Y, Yamakawa K. A nonsense mutation of the sodium channel gene SCN2A in a patient with intractable epilepsy and mental decline. J Neurosci 2004, 24:2690-2698.
23. Kang JQ, Macdonald RL. Making sense of nonsense GABAA receptor mutations associated with genetic epilepsies. Trends Mol Med 2009, 15:430-438.
24. Kearney JA, Plummer NW, Smith MR, Kapur J, Cummins TR, Waxman SG, Goldin AL, Meisler MH. A gain-of-function mutation in the sodium channel gene Scn2a results in seizures and behavioural abnormalities. Neuroscience 2001, 102:307-317.
25. Kearney JA, Wiste AK, Stephani U, Trudeau MM, Siegel A, RamachandranNair R, Elterman RD, Muhle H, Reinsdorf J, Shields WD, Meisler MH, Escayg A. Recurrent de novo mutations of SCN1A in severe myoclonic epilepsy of infancy. Pediatr Neurol 2006a, 34:116-120.
26. Kearney JA, Meisler MH. Single gene mutations in inherited and sporadic epilepsy. Encyclopedia of Basic Epilepsy Research 2009, In, Elsevier/Academic Press, London
27. Kearney JA, Yang Y, Beyer B, Bergren SK, Claes L, Dejonghe P, Frankel WN. Severe epilepsy resulting from genetic interaction between Scn2a and Kcnq2. Hum Mol Genet 2006b, 15:1043-1048.
28. Lossin C. A catalog of SCN1A variants. Brain Dev 2009, 31:114-130.
29. Madia F, Striano P, Gennaro E, Malacarne M, Paravidino R, Biancheri R, Budetta M, Cilio MR, Gaggero R, Pierluigi M, Minetti C, Zara F. Cryptic chromosome deletions involving SCN1A in severe myoclonic epilepsy of infancy. Neurology 2006, 67:1230-1235.
30. Maier SK, Westenbroek RE, Yamanushi TT, Dobrzynski H, Boyett MR, Catterall WA, Scheuer T. An unexpected requirement for brain-type sodium channels for control of heart rate in the mouse sinoatrial node. Proc Natl Acad Sci U S A 2003, 100:3507-3512.
31. Marini C, Scheffer IE, Nabbout R, Mei D, Cox K, Dibbens LM, McMahon JM, Iona X, Carpintero RS, Elia M, Cilio MR, Specchio N, Giordano L, Striano P, Gennaro E, Cross JH, Kivity S, Neufeld MY, Afawi Z, Andermann E, Keene D, Dulac O, Zara F, Berkovic SF, Guerrini R, Mulley JC. SCN1A duplications and deletions detected in Dravet syndrome: Implications for molecular diagnosis. Epilepsia 2010
32. Martin MS, Tang B, Papale LA, Yu FH, Catterall WA, Escayg A. The voltage-gated sodium channel Scn8a is a genetic modifier of severe myoclonic epilepsy of infancy. Hum Mol Genet 2007, 16:2892-2899.
33. Martin MS, Dutt K, Papale LA, Dube CM, Dutton SB, de Haan G, Shankar A, Tufik S, Meisler MH, Baram TZ, Goldin AL, Escayg A. Altered function of the SCN1A voltage-gated sodium channel leads to GABAergic interneuron abnormalities. J Biol Chem 2010, 285:9823-2834.
34. Meisler MH, Kearney JA. Sodium channel mutations in epilepsy and other neurological disorders. J Clin Investig 2005, 115:2010-2017.
35. Misra SN, Kahlig KM, George AL. Impaired NaV1.2 function and reduced cell surface expression in benign familial neonatal-infantile seizures. Epilepsia 2008, 49:1535-1545.
36. Nassar MA, Baker MD, Levato A, Ingram R, Mallucci G, McMahon SB, Wood JN. Nerve injury induces robust allodynia and ectopic discharges in Nav1.3 null mutant mice. Mol Pain 2006, 2:33.
37. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH, Wood JN. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 2004, 101:12706-12711.
38. 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 αII gene SCN2A in intractable epilepsies. Neurology 2009, 73:1046-1053.
39. Ogiwara I, Miyamoto H, Morita N, Atapour N, Mazaki E, Inoue I, Takeuchi T, Itohara S, Yanagawa Y, Obata K, Furuichi T, Hensch TK, Yamakawa K. 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.
40. Papale LA, Beyer B, Jones JM, Sharkey LM, Tufik S, Epstein M, Letts VA, Meisler MH, Frankel WN, 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.
41. Patino GA, Claes LR, Lopez-Santiago LF, Slat EA, Dondeti RS, Chen C, O'Malley HA, Gray CB, Miyazaki H, Nukina N, Oyama F, De Jonghe P, Isom LL. A functional null mutation of SCN1B in a patient with Dravet syndrome. J Neurosci 2009, 29:10764-10778.
42. Pereira S, Vieira JP, Barroca F, Roll P, Carvalhas R, Cau P, Sequeira S, Genton P, Szepetowski P. Severe epilepsy, retardation, and dysmorphic features with a 2q deletion including SCN1A and SCN2A. Neurology 2004, 63:191-192.
43. Planells-Cases R, Caprini M, Zhang J, Rockenstein EM, Rivera RR, Murre C, Masliah E, Montal M. Neuronal death and perinatal lethality in voltage-gated sodium channel αII-deficient mice. Biophys J 2000, 78:2878-2891.
44. Plummer NW, McBurney MW, Meisler MH. Alternative splicing of the sodium channel SCN8A predicts a truncated two-domain protein in fetal brain and non-neuronal cells. J Biol Chem 1997, 272:24008-24015.
45. Scheffer IE, Berkovic SF. Temporal lobe epilepsy and GEFS+ phenotypes associated with SCN1B mutations. Brain 2007, 130:100-109.
46. Shi X, Yasumoto S, Nakagawa E, Fukasawa T, Uchiya S, Hirose S. Missense mutation of the sodium channel gene SCN2A causes Dravet syndrome. Brain Dev 2009, 31:758-762.
47. Singh NA, Pappas C, Dahle EJ, Claes LR, Pruess TH, De Jonghe P, Thompson J, Dixon M, Gurnett C, Peiffer A, White HS, Filloux F, Leppert MF. A role of SCN9A in human epilepsies, as a cause of febrile seizures and as a potential modifier of Dravet syndrome. PLoS Genet 2009, 5:e1000649.
48. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, Blak A, Cooper O, Mitalipova M, Isacson O, Jaenisch R. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 2009, 136:964-977.
49. Suls A, Claeys KG, Goossens D, Harding B, Van Luijk R, Scheers S, Deprez L, Audenaert D, Van Dyck T, Beeckmans S, Smouts I, Ceulemans B, Lagae L, Buyse G, Barisic N, Misson JP, Wauters J, Del-Favero J, De Jonghe P, Claes LR. Microdeletions involving the SCN1A gene may be common in SCN1A-mutation-negative SMEI patients. Human Mutat 2006, 27:914-920.
50. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
51. Tang B, Escayg A. A BAC transgenic mouse model reveals neuron subtype-specific effects of a Generalized Epilepsy with Febrile Seizures Plus (GEFS+) mutation. Neurobiology of Disease 2009, 35:91-102.
52. Trudeau MM, Dalton JC, Day JW, Ranum LP, Meisler MH. 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.
53. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
54. Wallace RH, Wang DW, Singh R, Scheffer IE, George AL, Phillips HA, Saar K, Reis A, Johnson EW, Mulley JC. Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel beta1 subunit gene SCN1B. Nat genet 1998, 19:366-370.
55. Wallace RH, Scheffer IE, Parasivam G, Barnett S, Wallace GB, Sutherland GR, Berkovic SF, Mulley JC. Generalized epilepsy with febrile seizures plus: mutation of the sodium channel subunit SCN1B. Neurology 2002, 58:1426-1429.
56. Wang J, Ou SW, Wang YJ, Kameyama M, Kameyama A, Zong ZH. Analysis of four novel variants of Nav1.5/SCN5A cloned from the brain. Neurosci Res 2009, 64:339-347.
57. Whitaker WR, Clare JJ, Powell AJ, Chen YH, Faull RL, Emson PC. Distribution of voltage-gated sodium channel α-subunit and β-subunit mRNAs in human hippocampal formation, cortex, and cerebellum. J Comp Neurol 2000, 422:123-139.
58. Yamakawa K. Epilepsy and sodium channel gene mutations: gain or loss of function?. Neuroreport 2005, 16:1-3.
59. Yu FH, Mantegazza M, Westenbroek RE, Robbins CA, Kalume F, Burton KA, Spain WJ, McKnight GS, Scheuer T, Catterall WA. Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat Neurosci 2006, 9:1142-1149.