Nav1.1 haploinsufficiency in excitatory neurons ameliorates seizure-associated sudden death in a mouse model of dravet syndrome

Human Molecular Genetics

Volumn 22, Issue 23, 2013, Pages 4784-4804

  Ogiwara, Ikuo ^a   Iwasato, Takuji ^a,b,c   Miyamoto, Hiroyuki ^a,d   Iwata, Ryohei ^b,c   Yamagata, Tetsushi ^a   Mazaki, Emi ^a   Yanagawa, Yuchio ^d,e   Tamamaki, Nobuaki ^f   Hensch, Takao K ^a,g,h   Itohara, Shigeyoshi ^a,d   Yamakawa, Kazuhiro ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f KUMAMOTO UNIVERSITY   (Japan)

^g HARVARD UNIVERSITY   (United States)

^h BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; SODIUM CHANNEL NAV1.1;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; FEMALE; FOREBRAIN; FUNCTIONAL DISEASE; GENE DELETION; GENE TARGETING; HAPLOINSUFFICIENCY; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NERVE CELL; NONHUMAN; PREMATURE MORTALITY; PRIORITY JOURNAL; SEIZURE; SEVERE MYOCLONIC EPILEPSY IN INFANCY; SUDDEN DEATH; THALAMOCORTICAL TRACT; WESTERN BLOTTING;

ANIMALS; DEATH, SUDDEN; DISEASE MODELS, ANIMAL; EPILEPSIES, MYOCLONIC; HAPLOINSUFFICIENCY; INTERNEURONS; MICE; MUTATION; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; PARVALBUMINS;

EID: 84887553241     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt331     Document Type: Article

References (61)

1. Escayg, A., MacDonald, B.T., Meisler, M.H., Baulac, S., Huberfeld, G., An-Gourfinkel, I., Brice, A., LeGuern, E., Moulard, B., Chaigne, D. et al. (2000) Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat. Genet., 24, 343-345.
2. Claes, L., Del-Favero, J., Ceulemans, B., Lagae, L., Van Broeckhoven, C. and De Jonghe, P. (2001) De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy. Am. J. Hum. Genet., 68, 1327-1332.
3. Sugawara, T., Mazaki-Miyazaki, E., Ito, M., Nagafuji, H., Fukuma, G., Mitsudome, A., Wada, K., Kaneko, S., Hirose, S. and Yamakawa, K. (2001) Nav1.1 mutations cause febrile seizures associated with afebrile partial seizures. Neurology, 57, 703-705.
4. Sugawara, T., Mazaki-Miyazaki, E., Fukushima, K., Shimomura, J., Fujiwara, T., Hamano, S., Inoue, Y. and Yamakawa, K. (2002) Frequent mutations ofSCN1Ain severe myoclonic epilepsy in infancy. Neurology, 58, 1122-1124.
5. Fujiwara, T., Sugawara, T., Mazaki-Miyazaki, E., Takahashi, Y., Fukushima, K., Watanabe, M., Hara, K., Morikawa, T., Yagi, K., Yamakawa, K. et al. (2003) Mutations of sodium channel a subunit type 1 (SCN1A) in intractable childhood epilepsies with frequent generalized tonic-clonic seizures. Brain, 126, 531-546.
6. Harkin, L.A.,McMahon,J.M., Iona, X., Dibbens, L., Pelekanos, J.T., Zuberi, S.M., Sadleir, L.G., Andermann, E., Gill, D., Farrell, K. et al. (2007) The spectrum ofSCN1A-related infantile epileptic encephalopathies. Brain, 130, 843-852.
7. Depienne, C., Trouillard, O., Saint-Martin, C., An, I., Bouteiller, D., Carpentier, W., Keren, B., Abert, B., Gautier, A., Baulac, S. et al. (2009) Spectrum of SCN1A gene mutations associated with Dravet syndrome: analysis of 333 patients. J. Med. Genet., 46, 183-191.
8. Nakayama, T., Ogiwara, I., Ito, K., Kaneda, M., Mazaki, E., Osaka, H., Ohtani, H., Inoue, Y., Fujiwara, T., Uematsu, M. et al. (2010) Deletions of SCN1A 5′ genomic region with promoter activity in Dravet syndrome. Hum. Mut., 31, 820-829.
9. Engel, J. Jr (2001) A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia, 42, 796-803.
10. Dravet, C., Bureau, M., Oguni, H., Fukuyama, Y. and Cokar, O. (2005) Severe myoclonic epilepsy in infancy (Dravet syndrome). In Roger, J., Bureau, M., Dravet, C., Genton, P., Tassinari, C.A. and Wolf, P. (eds), Epileptic Syndromes in Infancy, Childhood and Adolescence, 4th edn. John Libbey Eurotext Ltd, Montrouge, France, pp. 89-113.
11. Sugawara, T., Tsurubuchi, Y., Fujiwara, T., Mazaki-Miyazaki, E., Nagata, K., Montal, M., Inoue, Y. and Yamakawa, K. (2003) Nav1.1 channels with mutations of severe myoclonic epilepsy in infancy display attenuated currents. Epilepsy Res., 54, 201-207.
12. Meisler, M.H. and Kearney, J.A. (2005) Sodium channel mutations in epilepsy and other neurological disorders. J. Clin. Invest., 115, 2010-2017.
13. Mulley, J.C., Scheffer, I.E., Petrou, S., Dibbens, L.M., Berkovic, S.F. and Harkin, L.A. (2005) SCN1A mutations and epilepsy. Hum. Mutat., 25, 535-542.
14. Yu, F.H., Mantegazza, M., Westenbroek, R.E., Robbins, C.A., Kalume, F., Burton, K.A., Spain, W.J., McKnight, G.S., Scheuer, T. and Catterall, W.A. (2006) Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat. Neurosci., 9, 1142- 1149.
15. Ogiwara, I., Miyamoto, H., Morita, N., Atapour, N., Mazaki, E., Inoue, I., Takeuchi, T., Itohara, S., Yanagawa, Y., Obata, K. et al. (2007) 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., 27, 5903-5914.
16. 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.
17. Ito, S., Ogiwara, I., Yamada, K., Miyamoto, H., Hensch, T.K., Osawa, M. and Yamakawa, K. (2013) Mouse with Nav1.1 haploinsufficiency, a model for Dravet syndrome, exhibits lowered sociability and learning impairment. Neurobiol. Dis., 49, 29-41.
18. Dutton, S.B., Makinson, C.D., Papale, L.A., Shankar, A., Balakrishnan, B., Nakazawa, K. and Escayg, A. (2013) Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiol. Dis., 49, 211-220.
19. Cheah, C.S., Yu, F.H., Westenbroek, R.E., Kalume, F.K., Oakley, J.C., Potter, G.B., Rubenstein, J.L. and Catterall, W.A. (2012) 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, 109, 14646-14651.
20. Potter, G.B., Petryniak, M.A., Shevchenko, E., McKinsey, G.L., Ekker, M. and Rubenstein, J.L. (2009) Generation of Cre-transgenic mice using Dlx1/ Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell. Neurosci., 40, 167-186.
21. Belforte, J.E., Zsiros, V., Sklar, E.R., Jiang, Z., Yu, G., Li, Y., Quinlan, E.M. and Nakazawa, K. (2010) Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat. Neurosci., 13, 76-83.
22. Lakso, M., Pichel, J.G., Gorman, J.R., Sauer, B., Okamoto, Y., Lee, E., Alt, F.W. and Westphal, H. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl Acad. Sci. USA, 93, 5860-5865.
23. Chaudhry, F.A., Reimer, R.J., Bellocchio, E.E., Danbolt, N.C., Osen, K.K., Edwards, R.H. and Storm-Mathisen, J. (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J. Neurosci., 18, 9733-9750.
24. Wojcik, S.M., Katsurabayashi, S., Guillemin, I., Friauf, E., Rosenmund, C., Brose, N. and Rhee, J.S. (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron, 50, 575-587.
25. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
26. Iwasato, T., Inan, M., Kanki, H., Erzurumlu, R.S., Itohara, S. and Crair, M.C. (2008) Cortical adenylyl cyclase 1 is required for thalamocortical synapse maturation and aspects of layer IV barrel development. J. Neurosci., 28, 5931-5943.
27. Chan, C.H., Godinho, L.N., Thomaidou, D., Tan, S.S., Gulisano, M. and Parnavelas, J.G. (2001) Emx1 is a marker for pyramidal neurons of the cerebral cortex. Cereb. Cortex, 11, 1191-1198.
28. Gorski, J.A., Talley, T., Qiu, M., Puelles, L., Rubenstein, J.L. and Jones, K.R. (2002) Cortical excitatory neurons and glia, but notGABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci., 22, 6309-6314.
29. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K. and Kaneko, T. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol., 467, 60-79.
30. Tamamaki, N. and Nojyo, Y. (1993) Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus, 3, 471-480.
31. Witter, M.P. (2007) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog. Brain Res., 163, 43-61.
32. van Groen, T., Miettinen, P. and Kadish, I. (2003) The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus, 13, 133-148.
33. Westenbroek, R.E., Merrick, D.K. and Catterall, W.A. (1989) Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron, 3, 695-704.
34. Gong, B., Rhodes, K.J., Bekele-Arcuri, Z. and Trimmer, J.S. (1999) Type I and type II Na+ channel a-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J. Comp. Neurol., 412, 342-352.
35. 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.
36. Lorincz, A. and Nusser, Z. (2008) Cell-type-dependent molecular composition of the axon initial segment. J. Neurosci., 28, 14329-14340.
37. Lorincz, A. and Nusser, Z. (2010) Molecular identity of dendritic voltage-gated sodium channels. Science, 328, 906-909.
38. Petreanu, L., Huber, D., Sobczyk, A. and Svoboda, K. (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci., 10, 663-668.
39. Feldmeyer, D., Lübke, J. and Sakmann, B. (2006) Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J. Physiol., 575, 583-602.
40. Petreanu, L., Mao, T., Sternson, S.M. and Svoboda, K. (2009) The subcellular organization of neocortical excitatory connections. Nature, 457, 1142-1145.
41. Herkenham, M. (1980) Laminar organization of thalamic projections to the rat neocortex. Science, 207, 532-535.
42. Tanahira, C., Higo, S., Watanabe, K., Tomioka, R., Ebihara, S., Kaneko, T. and Tamamaki, N. (2009) Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice. Neurosci. Res., 63, 213-223.
43. Bergmann, I., Nitsch, R. and Frotscher, M. (1991) Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anat. Embryol. (Berl.), 184, 403-409.
44. del Ri{dotless}́o, J.A., de Lecea, L., Ferrer, I. and Soriano, E. (1994) The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Brain Res. Dev. Brain Res., 81, 247-259.
45. de Lecea, L., del Ri{dotless}́o, J.A. and Soriano, E. (1995) Developmental expression of parvalbumin mRNA in the cerebral cortex and hippocampus of the rat. Brain Res. Mol. Brain Res., 32, 1-13.
46. Bishop, G.A. (1993) An analysis of HRP-filled basket cell axons in the cat's cerebellum. I. Morphometry and configuration. Anat. Embryol. (Berl.), 188, 287-297.
47. Sugihara, I., Fujita, H., Na, J., Quy, P.N., Li, B.Y. and Ikeda, D. (2009) Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolaseCcompartments of the rat cerebellum. J. Comp. Neurol., 512, 282-304.
48. Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D.R. and Arber, S. (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol., 3, e159.
49. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R. et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 13, 133-140.
50. Wen, L., Lu, Y.S., Zhu, X.H., Li, X.M., Woo, R.S., Chen, Y.J., Yin, D.M., Lai, C., Terry, A.V. Jr, Vazdarjanova, A. et al. (2010) Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl Acad. Sci. USA, 107, 1211-1216.
51. Atallah, B.V., Bruns, W., Carandini, M. and Scanziani, M. (2012) Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron, 73, 159-170.
52. Shamir, A., Kwon, O.B., Karavanova, I., Vullhorst, D., Leiva-Salcedo, E., Janssen, M.J. and Buonanno, A. (2012)The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J. Neurosci., 32, 2988-2997.
53. Freund, T.F. and Buzsáki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347-470.
54. Klausberger, T., Magill, P.J., Márton, L.F., Roberts, J.D., Cobden, P.M., Buzsáki, G. and Somogyi, P. (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature, 421, 844-848.
55. Gulyás, A.I., Szabó, G.G., Ulbert, I., Holderith, N., Monyer, H., Erdélyi, F., Szabó, G., Freund, T.F. and Hájos, N. (2010) Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J. Neurosci., 30, 15134- 15145.
56. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475.
57. Paz, J.T., Davidson, T.J., Frechette, E.S., Delord, B., Parada, I., Peng, K., Deisseroth, K. and Huguenard, J.R. (2013) Closed-loop optogenetic control of thalamus as a new tool to interrupt seizures after cortical injury. Nat. Neurosci., 16, 64-70.
58. Kanki, H., Suzuki, H. and Itohara, S. (2006) High-efficiency CAG-FLPe deleter mice in C57BL/6J background. Exp. Anim., 55, 137-141.
59. Iwasato, T., Katoh, H., Nishimaru, H., Ishikawa, Y., Inoue, H., Saito, Y.M., Ando, R., Iwama, M., Takahashi, R., Negishi, M. et al. (2007) Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell, 130, 742-753.
60. Iwasato, T., Nomura, R., Ando, R., Ikeda, T., Tanaka, M. and Itohara, S. (2004) Dorsal telencephalon-specific expression of Cre recombinase inPAC transgenic mice. Genesis, 38, 130-138.
61. Iwasato, T., Datwani, A., Wolf, A.M., Nishiyama, H., Taguchi, Y., Tonegawa, S., Knöpfel, T., Erzurumlu, R.S. and Itohara, S. (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature, 406, 726-731.