CRISPR/Cas9 facilitates investigation of neural circuit disease using human iPSCs: Mechanism of epilepsy caused by an SCN1A loss-of-function mutation

Translational Psychiatry

Volumn 6, Issue , 2016, Pages

  Liu, J ^a,b   Gao, C ^b   Chen, W ^b   Ma, W ^b   Li, X ^b   Shi, Y ^c   Zhang, H ^b   Zhang, L ^b   Long, Y ^b   Xu, H ^b   Guo, X ^b   Deng, S ^d   Yan, X ^d   Yu, D ^b   Pan, G ^b   Chen, Y ^b   Lai, L ^b   Liao, W ^c   Li, Z ^b,d  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

^d CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; SODIUM CHANNEL NAV1.1; SCN1A PROTEIN, HUMAN;

ARTICLE; CASE REPORT; COMPLEX PARTIAL SEIZURE; CRISPR CAS SYSTEM; CRISPR CAS9; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; EPILEPSY; EPILEPTOGENESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEBRILE CONVULSION; FOCAL EPILEPSY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MALE; MISSENSE MUTATION; MOSAICISM; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; PHENOTYPE; PLURIPOTENT STEM CELL; TONIC CLONIC SEIZURE; ANIMAL; CELL CULTURE; CHILD; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; FEMALE; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOUSE; MUTATION;

ANIMALS; CELLS, CULTURED; CHILD; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; ELECTROPHYSIOLOGICAL PHENOMENA; EPILEPSY; FEMALE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MUTATION; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; NERVE NET;

EID: 84953726026     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.203     Document Type: Article

References (43)

1. Catterall WA, Kalume F, Oakley JC. NaV1.1 channels and epilepsy. J Physiol 2010; 588: 1849-1859
2. Escayg A, MacDonald BT, Meisler MH, Baulac S, Huberfeld G, An-Gourfinkel I, et al. Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+. Nat Genet 2000; 24: 343-345
3. Dravet C. Dravet syndrome history. Dev Med Child Neurol 2011; 53: 1-6
4. Steinlein OK. Genetic mechanisms that underlie epilepsy. Nat Rev Neurosci 2004; 5: 400-408
5. Watanabe M, Fujiwara T, Yagi K, Seino M, Higashi T. Intractable childhood epilepsy with generalized tonic-clonic seizures. J Jpn Epil Soc 1989; 7: 96-105
6. Margolis JM, Chu BC, Wang ZJ, Copher R, Cavazos JE. Effectiveness of antiepileptic drug combination therapy for partial-onset seizures based on mechanisms of action. JAMA Neurol 2014; 71: 985-993
7. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr. Molecular basis of an inherited epilepsy. Neuron 2002; 34: 877-884
8. Lossin C, Rhodes TH, Desai RR, Vanoye CG, Wang D, Carniciu S, et al. Epilepsyassociated dysfunction in the voltage-gated neuronal sodium channel SCN1A. J Neurosci 2003; 23: 11289-11295
9. Sugawara T, Tsurubuchi Y, Fujiwara T, Mazaki-Miyazaki E, Ngata K, Montal M, et al. Nav1.1 channels with mutations of severe myoclonic epilepsyin infancy display attenuated currents. Epilepsy Res 2003; 54: 201-207
10. Rhodes TH, Lossin C, Vanoye CG, Wang DW, George AL Jr. Noninactivating voltage-gated sodium channels in severe myoclonic epilepsy of infancy. Proc Natl Acad Sci USA 2004; 101: 11147-11152
11. Ohmori I, Kahlig KM, Rhodes TH, Wang DW, George AL Jr. Nonfunctional SCN1A is common in severe myoclonic epilepsy of infancy. Epilepsia 2006; 47: 1636-1642
12. Mantegazza M, Rusconi R, Scalmani P, Avanzini G, Franceschetti S. Epileptogenic ion channel mutations: from bedside to bench and, hopefully, back again. Epilepsy Res 2010; 92: 1-29
13. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872
14. Shi Y, Kirwan P, Livesey FJ. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc 2012; 7: 1836-1846
15. Parent JM, Anderson SA. Reprogramming patient-derived cells to study the epilepsies. Nat Neurosci 2015; 18: 360-366
16. 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
17. Yu FH, Mantegazza M, Westenbroek RE, Robbins CA, Kalume F, Burton KA, et al. Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat Neurosci 2006; 9: 1142-1149
18. 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
19. Liu Y, Lopez-Santiago LF, Yuan Y, Jones JM, Zhang H, O'Malley HA, et al. Dravet syndrome patient-derived neurons suggest a novel epilepsy mechanism. Ann Neurol 2013; 74: 128-139
20. 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
21. Cheah CS, Yu FH, Westenbroek RE, Kalume FK, Oakley JC, Potter GB, 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 USA 2012; 109: 14646-14651
22. Dutton SB, Makinson CD, Papale LA, Shankar A, Balakrishnan B, Nakazawa K, et al. Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiol Dis 2013; 49: 211-220
23. Westenbroek RE, Merrick DK, Catterall WA. Differential subcellular localization of the RIand RIINa+ channel subtypes in central neurons. Neuron 1989; 3: 695-704
24. Scheffer IE, Berkovic SF. Generalized epilepsy with febrile seizures plus. A genetic disorder with heterogeneous clinical phenotypes. Brain 1997; 120: 479-490
25. Singh R, Andermann E, Whitehouse WP, Harvey AS, Keene DL, Seni MH, et al. Severe myoclonic epilepsy of infancy: extended spectrum of GEFS+. Epilepsia 2001; 42: 837-844
26. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 2011; 29: 143-148
27. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science 2013; 339: 823-826
28. Gaj T, Gersbach CA, Barbas CF 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 2013; 31: 397-405
29. Shi YW, Yu MJ, Long YS, Qin B, He N, Meng H, et al. Mosaic SCN1A mutations in familial partial epilepsy with antecedent febrile seizures. Genes Brain Behav 2012; 11: 170-176
30. Chen WJ, Liu JX, Zhang LM, Xu HJ, Guo XG, Deng SH, et al. Generation of the SCN1A epilepsy mutation in hiPS cells using the TALEN technique. Sci Rep 2014; 4: 5404
31. Thompson CH, Porter JC, Kahlig KM, Daniels MA, George AL Jr. Nontruncating SCN1A mutations associated with severe myoclonic epilepsy of infancy impair cell surface expression. J Biol Chem 2012; 287: 42001-42008
32. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K, et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012; 149: 708-721
33. Jiao J, Yang Y, Shi Y, Chen J, Gao R, Fan Y, et al. Modeling Dravet syndrome using induced pluripotent stem cells (iPSCs) and directly converted neurons. Hum Mol Genet 2013; 22: 4241-4252
34. Zhang SC, Wernig M, Duncan ID, Brustle O, Thomson JA. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001; 19: 1129-1133
35. Pankratz MT, Li XJ, Lavaute TM, Lyons EA, Chen X, Zhang SC. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007; 25: 1511-1520
36. Johnson MA, Weick JP, Pearce RA, Zhang SC. Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci 2007; 27: 3069-3077
37. Li XJ, Zhang X, Johnson MA, Wang ZB, Lavaute T, Zhang SC. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 2009; 136: 4055-4063
38. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse.J Comp Neurol 2003; 60-79
39. Abriel H, Kass RS. Regulation of the voltage-gated cardiac sodium channel Nav1.5 by interacting proteins. Trends Cardiovasc Med 2005; 15: 35-40
40. Rusconi R, Scalmani P, Cassulini RR, Giunti G, Gambardella A, Franceschetti S, et al. Modulatory proteins can rescue a trafficking defective epileptogenic Nav1.1 Na+ channel mutant. J Neurosci 2007; 27: 11037-11046
41. Gilchrist J, Dutton S, Diaz-Bustaman M, McPherson A, Olivares N, Kalia J, et al. Nav1.1 modulation by a novel triazole compound attenuates epileptic seizures in rodents. ACS Chem Biol 2014; 9: 1204-1212
42. St Louis EK. Truly ?rational? polytherapy: maximizing efficacy and minimizing drug interactions, drug load, and adverse effects. Curr Neuropharmacol 2009; 7: 96-105
43. Letinic K, Zoncu R, Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 2002; 417: 645-649