A deleterious Nav1.1 mutation selectively impairs telencephalic inhibitory neurons derived from Dravet Syndrome patients

eLife

Volumn 5, Issue 2016JULY, 2016, Pages

  Sun, Yishan ^a,b   Paşca, Sergiu P ^b   Portmann, Thomas ^b,d   Goold, Carleton ^a,b   Worringer, Kathleen A ^a   Guan, Wendy ^a   Chan, Karen C ^b   Gai, Hui ^b   Vogt, Daniel ^c   Chen, Ying Jiun J ^c   Mao, Rong ^b   Chan, Karrie ^a   Rubenstein, John L R ^c   Madison, Daniel V ^b   Hallmayer, Joachim ^b   Froehlich Santino, Wendy M ^b   Bernstein, Jonathan A ^b   Dolmetsch, Ricardo E ^a,b  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Circuit Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHANNEL NAV1.1; SCN1A PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; CYTOGENETICS; GENE DELETION; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; HYPERSENSITIVITY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MEDIAN EMINENCE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERE MYOCLONIC EPILEPSY IN INFANCY; SKIN BIOPSY; WESTERN BLOTTING; CELL CULTURE; DEFICIENCY; GENETICS; INDUCED PLURIPOTENT STEM CELL; MUTATION; MYOCLONUS EPILEPSY; NERVE CELL; PATHOLOGY; PHYSIOLOGY; TELENCEPHALON;

CELLS, CULTURED; EPILEPSIES, MYOCLONIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MUTATION; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; TELENCEPHALON;

EID: 84979520533     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13073     Document Type: Article

References (54)

1. Cai Y, Zhang Q, Wang C, Zhang Y, Ma T, Zhou X, Tian M, Rubenstein JL, Yang Z. 2013. Nuclear receptor COUP-TFII-expressing neocortical interneurons are derived from the medial and lateral/caudal ganglionic eminence and define specific subsets of mature interneurons. Journal of Comparative Neurology 521: 479-497. doi: 10. 1002/cne.23186
2. Catterall WA, Kalume F, Oakley JC. 2010. NaV1.1 channels and epilepsy. Journal of Physiology 588: 1849-1859. doi: 10.1113/jphysiol.2010.187484
3. Cestè le S, Scalmani P, Rusconi R, Terragni B, Franceschetti S, Mantegazza M. 2008. Self-limited hyperexcitability: functional effect of a familial hemiplegic migraine mutation of the Nav1.1 (SCN1A) Na+ channel. Journal of Neuroscience 28: 7273-7283. doi: 10.1523/JNEUROSCI.4453-07.2008
4. Cestè le S, Schiavon E, Rusconi R, Franceschetti S, Mantegazza M. 2013. Nonfunctional NaV1.1 familial hemiplegic migraine mutant transformed into gain of function by partial rescue of folding defects. Proceedings of the National Academy of Sciences of the United States of America 110: 17546-17551. doi: 10.1073/pnas. 1309827110
5. Cheah CS, Yu FH, Westenbroek RE, Kalume FK, Oakley JC, Potter GB, Rubenstein JL, Catterall WA. 2012. Specific deletion of NaV1.1 sodium channels in inhibitory interneurons causes seizures and premature death in a mouse model of Dravet syndrome. Proceedings of the National Academy of Sciences of the United States of America 109: 14646-14651. doi: 10.1073/pnas.1211591109
6. Chen YJ, Vogt D, Wang Y, Visel A, Silberberg SN, Nicholas CR, Danjo T, Pollack JL, Pennacchio LA, Anderson S, Sasai Y, Baraban SC, Kriegstein AR, Alvarez-Buylla A, Rubenstein JL. 2013. Use of "MGE enhancers" for labeling and selection of embryonic stem cell-derived medial ganglionic eminence (MGE) progenitors and neurons. PLOS One 8: e61956. doi: 10.1371/journal.pone.0061956
7. Danjo T, Eiraku M, Muguruma K, Watanabe K, Kawada M, Yanagawa Y, Rubenstein JL, Sasai Y. 2011. Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed and combinatory treatment with extrinsic signals. Journal of Neuroscience 31: 1919-1933. doi: 10.1523/JNEUROSCI.5128-10.2011
8. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie TW, Helmchen F, Denk W, Brecht M, Osten P. 2004. Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proceedings of the National Academy of Sciences of the United States of America 101: 18206-18211. doi: 10.1073/pnas.0407976101
9. Donnelly ML, Hughes LE, Luke G, Mendoza H, ten Dam E, Gani D, Ryan MD. 2001. The ‘cleavage’ activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring '2A-like’ sequences. Journal of General Virology 82: 1027-1041. doi: 10.1099/0022-1317-82-5-1027
10. Dravet C, Bureau M, Dalla Bernardina B, Guerrini R. 2011. Severe myoclonic epilepsy in infancy (Dravet syndrome) 30 years later. Epilepsia 52 Suppl 2: 1-2. doi: 10.1111/j.1528-1167.2011.02993.x
11. Dravet C. 2011. The core Dravet syndrome phenotype. Epilepsia 52 Suppl 2: 3-9. doi: 10.1111/j.1528-1167.2011.02994.x
12. Dutton SB, Makinson CD, Papale LA, Shankar A, Balakrishnan B, Nakazawa K, Escayg A. 2013. Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiology of Disease 49: 211-220. doi: 10.1016/j.nbd.2012.08.012
13. Escayg A, Goldin AL. 2010. Sodium channel SCN1A and epilepsy: mutations and mechanisms. Epilepsia 51: 1650-1658. doi: 10.1111/j.1528-1167.2010.02640.x
14. Fogarty M, Grist M, Gelman D, Marín O, Pachnis V, Kessaris N. 2007. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. Journal of Neuroscience 27: 10935-10981. doi: 10.1523/JNEUROSCI.1629-07.2007
15. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. 2009. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proceedings of the Japan Academy, Series B 85: 348-362. doi: 10.2183/pjab.85.348
16. Goulburn AL, Stanley EG, Elefanty AG, Anderson SA. 2012. Generating GABAergic cerebral cortical interneurons from mouse and human embryonic stem cells. Stem Cell Research 8: 416-426. doi: 10.1016/j.scr.2011.12.002
17. Hanson JE, Orr AL, Fernandez-Illescas S, Valenzuela RA, Madison DV. 2010. Hippocampal Slice Cultures. In: Doering L. C, (Ed) Protocols for Neural Cell Culture. 4th ed. New York, NY: Springer. p299-311.
18. Higurashi N, Uchida T, Lossin C, Misumi Y, Okada Y, Akamatsu W, Imaizumi Y, Zhang B, Nabeshima K, Mori MX, Katsurabayashi S, Shirasaka Y, Okano H, Hirose S. 2013. A human Dravet syndrome model from patient induced pluripotent stem cells. Molecular Brain 6: 19. doi: 10.1186/1756-6606-6-19
19. Hussein SM, Batada NN, Vuoristo S, Ching RW, Autio R, NärväE, Ng S, Sourour M, Hämäläinen R, Olsson C, Lundin K, Mikkola M, Trokovic R, Peitz M, Brüstle O, Bazett-Jones DP, Alitalo K, Lahesmaa R, Nagy A, Otonkoski T. 2011. Copy number variation and selection during reprogramming to pluripotency. Nature 471: 58-62. doi: 10.1038/nature09871
20. Jiao J, Yang Y, Shi Y, Chen J, Gao R, Fan Y, Yao H, Liao W, Sun XF, Gao S. 2013. Modeling Dravet syndrome using induced pluripotent stem cells (iPSCs) and directly converted neurons. Human Molecular Genetics 22: 4241-4252. doi: 10.1093/hmg/ddt275
21. Kalume F, Yu FH, Westenbroek RE, Scheuer T, Catterall WA. 2007. Reduced sodium current in Purkinje neurons from Nav1.1 mutant mice: implications for ataxia in severe myoclonic epilepsy in infancy. Journal of Neuroscience 27: 11065-11074. doi: 10.1523/JNEUROSCI.2162-07.2007
22. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. 2010. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. Journal of Neuroscience 30: 16796-17604. doi: 10.1523/JNEUROSCI.1869-10.2010
23. Liu J, Gao C, Chen W, Ma W, Li X, Shi Y, Zhang H, Zhang L, Long Y, Xu H, Guo X, Deng S, Yan X, Yu D, Pan G, Chen Y, Lai L, Liao W, Li Z. 2016. CRISPR/Cas9 facilitates investigation of neural circuit disease using human iPSCs: mechanism of epilepsy caused by an SCN1A loss-of-function mutation. Translational Psychiatry 6: e703. doi: 10.1038/tp.2015.203
24. Liu Y, Lopez-Santiago LF, Yuan Y, Jones JM, Zhang H, O’Malley HA, Patino GA, O’Brien JE, Rusconi R, Gupta A, Thompson RC, Natowicz MR, Meisler MH, Isom LL, Parent JM. 2013. Dravet syndrome patient-derived neurons suggest a novel epilepsy mechanism. Annals of Neurology 74: 128-139. doi: 10.1002/ana.23897
25. Lorincz A, Nusser Z. 2008. Cell-type-dependent molecular composition of the axon initial segment. Journal of Neuroscience 28: 14329-14340. doi: 10.1523/JNEUROSCI.4833-08.2008
26. Ma T, Wang C, Wang L, Zhou X, Tian M, Zhang Q, Zhang Y, Li J, Liu Z, Cai Y, Liu F, You Y, Chen C, Campbell K, Song H, Ma L, Rubenstein JL, Yang Z. 2013. Subcortical origins of human and monkey neocortical interneurons. Nature Neuroscience 16: 1588-1597. doi: 10.1038/nn.3536
27. Maroof AM, Brown K, Shi SH, Studer L, Anderson SA. 2010. Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells. Journal of Neuroscience 30: 4667-4675. doi: 10.1523/JNEUROSCI.4255-09.2010
28. Maroof AM, Keros S, Tyson JA, Ying SW, Ganat YM, Merkle FT, Liu B, Goulburn A, Stanley EG, Elefanty AG, Widmer HR, Eggan K, Goldstein PA, Anderson SA, Studer L. 2013. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12: 559-572. doi: 10.1016/j.stem.2013.04.008
29. Martin MS, Dutt K, Papale LA, Dubé CM, Dutton SB, de Haan G, Shankar A, Tufik S, Meisler MH, Baram TZ, Goldin AL, Escayg A. 2010. Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. Journal of Biological Chemistry 285: 9823-9834. doi: 10.1074/jbc.M109.078568
30. McCarthy KD, de Vellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. Journal of Cell Biology 85: 890-902. doi: 10.1083/jcb.85.3.890
31. Mistry AM, Thompson CH, Miller AR, Vanoye CG, George AL, Kearney JA. 2014. Strain-and age-dependent hippocampal neuron sodium currents correlate with epilepsy severity in Dravet syndrome mice. Neurobiology of Disease 65: 1-11. doi: 10.1016/j.nbd.2014.01.006
32. Nicholas CR, Chen J, Tang Y, Southwell DG, Chalmers N, Vogt D, Arnold CM, Chen YJ, Stanley EG, Elefanty AG, Sasai Y, Alvarez-Buylla A, Rubenstein JL, Kriegstein AR. 2013. Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12: 573-586. doi: 10.1016/j.stem.2013.04.005
33. Ogiwara I, Iwasato T, Miyamoto H, Iwata R, Yamagata T, Mazaki E, Yanagawa Y, Tamamaki N, Hensch TK, Itohara S, Yamakawa K. 2013. Nav1.1 haploinsufficiency in excitatory neurons ameliorates seizure-associated sudden death in a mouse model of Dravet syndrome. Human Molecular Genetics 22: 4784-4804. doi: 10.1093/hmg/ddt331
34. 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. 2007. Nav1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. Journal of Neuroscience 27: 5903-5914. doi: 10.1523/JNEUROSCI.5270-06.2007
35. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB. 2009. Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. Journal of Neuroscience 29: 7040-7052. doi: 10. 1523/JNEUROSCI.0105-09.2009
36. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S, Hong H, Nakagawa M, Tanabe K, Tezuka K, Shibata T, Kunisada T, Takahashi M, Takahashi J, Saji H, Yamanaka S. 2011. A more efficient method to generate integration-free human iPS cells. Nature Methods 8: 409-412. doi: 10.1038/nmeth.1591
37. Paşca SP, Portmann T, Voineagu I, Yazawa M, Shcheglovitov A, Paşca AM, Cord B, Palmer TD, Chikahisa S, Nishino S, Bernstein JA, Hallmayer J, Geschwind DH, Dolmetsch RE, Pasca AM. 2011. Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nature Medicine 17: 1657-1662. doi: 10.1038/nm.2576
38. Paşca SP, Portmann T, Voineagu I, Yazawa M, Shcheglovitov A, Paşca AM, Cord B, Palmer TD, Chikahisa S, Nishino S, Bernstein JA, Hallmayer J, Geschwind DH, Dolmetsch RE. 2011. Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nature Medicine 17: 1657-1662. doi: 10.1038/nm.2576
39. Rubinstein M, Westenbroek RE, Yu FH, Jones CJ, Scheuer T, Catterall WA. 2015. Genetic background modulates impaired excitability of inhibitory neurons in a mouse model of Dravet syndrome. Neurobiology of Disease 73: 106-117. doi: 10.1016/j.nbd.2014.09.017
40. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Developmental Neurobiology 71: 45-61. doi: 10.1002/dneu.20853
41. Shcheglovitov A, Shcheglovitova O, Yazawa M, Portmann T, Shu R, Sebastiano V, Krawisz A, Froehlich W, Bernstein JA, Hallmayer JF, Dolmetsch RE. 2013. SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503: 267-271. doi: 10.1038/nature12618
42. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C, Huang ZJ, Nelson SB. 2006. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nature Neuroscience 9: 99-107. doi: 10.1038/nn1618
43. Sultan KT, Brown KN, Shi SH. 2013. Production and organization of neocortical interneurons. Frontiers in Cellular Neuroscience 7: 221. doi: 10.3389/fncel.2013.00221
44. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, Vignali DA. 2004. Correction of multi-gene deficiency in vivo using a single ‘self-cleaving’ 2A peptide-based retroviral vector. Nature Biotechnology 22: 589-594. doi: 10.1038/nbt957
45. Tai C, Abe Y, Westenbroek RE, Scheuer T, Catterall WA. 2014. Impaired excitability of somatostatin-and parvalbumin-expressing cortical interneurons in a mouse model of Dravet syndrome. Proceedings of the National Academy of Sciences of the United States of America 111: E3139-E3148. doi: 10.1073/pnas. 1411131111
46. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872. doi: 10.1016/j.cell.2007.11.019
47. Toresson H, Potter SS, Campbell K. 2000. Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127: 4361-4371.
48. Tsai MS, Lee ML, Chang CY, Fan HH, Yu IS, Chen YT, You JY, Chen CY, Chang FC, Hsiao JH, Khorkova O, Liou HH, Yanagawa Y, Lee LJ, Lin SW. 2015. Functional and structural deficits of the dentate gyrus network coincide with emerging spontaneous seizures in an Scn1a mutant Dravet Syndrome model during development. Neurobiology of Disease 77: 35-48. doi: 10.1016/j.nbd.2015.02.010
49. Vucurovic K, Gallopin T, Ferezou I, Rancillac A, Chameau P, van Hooft JA, Geoffroy H, Monyer H, Rossier J, Vitalis T. 2010. Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cerebral Cortex 20: 2333-2380. doi: 10.1093/cercor/bhp310
50. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nature Reviews Neuroscience 7: 687-696. doi: 10.1038/nrn1954
51. Yazawa M, Hsueh B, Jia X, Pasca AM, Bernstein JA, Hallmayer J, Dolmetsch RE. 2011. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 471: 230-234. doi: 10.1038/nature09855
52. Yu FH, Mantegazza M, Westenbroek RE, Robbins CA, Kalume F, Burton KA, Spain WJ, McKnight GS, Scheuer T, Catterall WA. 2006. Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nature Neuroscience 9: 1142-1149. doi: 10.1038/nn1754
53. Yun K, Potter S, Rubenstein JL. 2001. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128: 193-205.
54. Zhang Y, Pak C, Han Y, Ahlenius H, Zhang Z, Chanda S, Marro S, Patzke C, Acuna C, Covy J, Xu W, Yang N, Danko T, Chen L, Wernig M, Südhof TC. 2013. Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78: 785-883. doi: 10.1016/j.neuron.2013.05.029