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

Volumn 111, Issue 30, 2014, Pages

  Tai, Chao ^a   Abe, Yasuyuki ^a,b   Westenbroek, Ruth E ^a   Scheuer, Todd ^a   Catterall, William A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b DAIICHI SANKYO CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PARVALBUMIN; RHEOBASE; SODIUM; SODIUM CHANNEL NAV1.1; SOMATOSTATIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; EXCITABILITY; GABAERGIC SYSTEM; GENE MUTATION; HAPLOINSUFFICIENCY; INTERNEURON; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEVERE MYOCLONIC EPILEPSY IN INFANCY; SODIUM CURRENT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; DISEASE MODELS, ANIMAL; EPILEPSIES, MYOCLONIC; GABAERGIC NEURONS; GENE EXPRESSION REGULATION; MICE; MICE, MUTANT STRAINS; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; NEOCORTEX; PARVALBUMINS; PYRAMIDAL CELLS; SOMATOSTATIN;

EID: 84905011516     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1411131111     Document Type: Article

References (58)

1. Wolff M, Cassé-Perrot C, Dravet C (2006) Severe myoclonic epilepsy of infants (Dravet syndrome): Natural history and neuropsychological findings. Epilepsia 47(Suppl 2):45-48. (Pubitemid 44684620)
2. Genton P, Velizarova R, Dravet C (2011) Dravet syndrome: The long-term outcome. Epilepsia 52(Suppl 2):44-49.
3. Brunklaus A, Dorris L, Zuberi SM (2011) Comorbidities and predictors of health-related quality of life in Dravet syndrome. Epilepsia 52(8):1476-1482.
4. Claes L, et al. (2001) De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy. Am J Hum Genet 68(6):1327-1332. (Pubitemid 32510608)
5. Claes LR, et al. (2009) The SCN1A variant database: A novel research and diagnostic tool. Hum Mutat 30(10):E904-E920.
6. Rilstone JJ, Coelho FM, Minassian BA, Andrade DM (2012) Dravet syndrome: Seizure control and gait in adults with different SCN1A mutations. Epilepsia 53(8):1421-1428.
7. Akiyama M, Kobayashi K, Ohtsuka Y (2012) Dravet syndrome: A genetic epileptic disorder. Acta Med Okayama 66(5):369-376.
8. Yu FH, et al. (2006) Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat Neurosci 9(9):1142-1149. (Pubitemid 44306307)
9. Ogiwara I, 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(22):5903-5914. (Pubitemid 46849766)
10. 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. J Neurosci 27(41):11065-11074. (Pubitemid 47574172)
11. Oakley JC, Kalume F, Yu FH, Scheuer T, Catterall WA (2009) Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy. Proc Natl Acad Sci USA 106(10):3994-3999.
12. (V)1.1 channels are critical for intercellular communication in the suprachiasmatic nucleus and for normal circadian rhythms. Proc Natl Acad Sci USA 109(6):E368-E377.
13. Han S, et al. (2012) Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature 489(7416):385-390.
14. Kalume F, et al. (2013) Sudden unexpected death in a mouse model of Dravet syndrome. J Clin Invest 123(4):1798-1808.
15. V1.1 sodium channels in inhibitory interneurons causes seizures and premature death in a mouse model of Dravet syndrome. Proc Natl Acad Sci USA 109(36):14646-14651.
16. Markram H, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5(10):793-807. (Pubitemid 39336216)
17. Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71(1):45-61.
18. Ascoli GA, et al.; Petilla Interneuron Nomenclature Group (2008) Petilla terminology: Nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9(7):557-568. (Pubitemid 351873463)
19. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7(6):476-486. (Pubitemid 27353633)
20. Xu X, Roby KD, Callaway EM (2010) Immunochemical characterization of inhibitory mouse cortical neurons: Three chemically distinct classes of inhibitory cells. J Comp Neurol 518(3):389-404.
21. Hasenstaub A, et al. (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47(3):423-435. (Pubitemid 41073882)
22. Haider B, McCormick DA (2009) Rapid neocortical dynamics: Cellular and network mechanisms. Neuron 62(2):171-189.
23. Dutton SB, et al. (2012) Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiol Dis 49C:211-220.
24. Ogiwara I, et al. (2013) Nav1.1 haploinsufficiency in excitatory neurons ameliorates seizure-associated sudden death in a mouse model of Dravet syndrome. Hum Mol Genet 22(23):4784-4804.
25. Xu H, Jeong HY, Tremblay R, Rudy B (2013) Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77(1):155-167.
26. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26(19):5069-5082. (Pubitemid 44315288)
27. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53(5):735-746.
28. Berger TK, Perin R, Silberberg G, Markram H (2009) Frequency-dependent disynaptic inhibition in the pyramidal network: A ubiquitous pathway in the developing rat neocortex. J Physiol 587(Pt 22):5411-5425.
29. Murayama M, et al. (2009) Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457(7233):1137-1141.
30. Duflocq A, Le Bras B, Bullier E, Couraud F, Davenne M (2008) Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci 39(2):180-192.
31. + channel subtypes in central neurons. Neuron 3(6):695-704.
32. Goldberg EM, Coulter DA (2013) Mechanisms of epileptogenesis: A convergence on neural circuit dysfunction. Nat Rev Neurosci 14(5):337-349.
33. Wang Y, et al. (2004) Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561(Pt 1):65-90. (Pubitemid 39549467)
34. Pignatelli M, Beyeler A, Leinekugel X (2012) Neural circuits underlying the generation of theta oscillations. J Physiol Paris 106(3-4):81-92.
35. Benchenane K, Tiesinga PH, Battaglia FP (2011) Oscillations in the prefrontal cortex: A gateway to memory and attention. Curr Opin Neurobiol 21(3):475-485.
36. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M (2007) Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10(6):743-753. (Pubitemid 46828515)
37. Martin MS, et al. (2010) Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J Biol Chem 285(13):9823-9834.
38. Tang B, et al. (2009) A BAC transgenic mouse model reveals neuron subtype-specific effects of a Generalized Epilepsy with Febrile Seizures Plus (GEFS+) mutation. Neurobiol Dis 35(1):91-102.
39. Lorincz A, Nusser Z (2008) Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28(53):14329-14340.
40. Vacher H, Mohapatra DP, Trimmer JS (2008) Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol Rev 88(4):1407-1447.
41. Bartos M, Elgueta C (2012) Functional characteristics of parvalbumin- and cholecys-tokinin-expressing basket cells. J Physiol 590(Pt 4):669-681.
42. Dölen G, et al. (2007) Correction of fragile X syndrome in mice. Neuron 56(6):955-962. (Pubitemid 350251119)
43. Rossignol E (2011) Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast 2011:649325.
44. Verret L, et al. (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149(3):708-721.
45. V2.1 ablation in cortical interneurons selectively impairs fast-spiking basket cells and causes generalized seizures. Ann Neurol 74(2):209-222.
46. Zhou FW, Roper SN (2011) Altered firing rates and patterns in interneurons in experimental cortical dysplasia. Cereb Cortex 21(7):1645-1658.
47. Cobos I, et al. (2005) Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8(8):1059-1068. (Pubitemid 41061517)
48. Buchanan KA, et al. (2012) Target-specific expression of presynaptic NMDA receptors in neocortical microcircuits. Neuron 75(3):451-466.
49. Berger TK, Silberberg G, Perin R, Markram H (2010) Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol 8(9):8.
50. Liu Y, et al. (2013) Dravet syndrome patient-derived neurons suggest a novel epilepsy mechanism. Ann Neurol 74(1):128-139.
51. Higurashi N, et al. (2013) A human Dravet syndrome model from patient induced pluripotent stem cells. Mol Brain 6:19.
52. Banker G, Goslin K (1998) Culturing Nerve Cells (Massachusetts Institute of Technology, Boston, MA).
53. DeFelipe J, et al. (2013) New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14(3):202-216.
54. Wu Q, Chen M, Buchwald M, Phillips RA (1995) A simple, rapid method for isolation of high quality genomic DNA from animal tissues. Nucleic Acids Res 23(24):5087-5088. (Pubitemid 26012495)
55. Tamamaki N, et al. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467(1):60-79. (Pubitemid 37339758)
56. Chattopadhyaya B, et al. (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24(43):9598-9611. (Pubitemid 39441514)
57. Committee on Care and Use of Laboratory Animals (1985) Guide for the Care and Use of Laboratory Animals (Natl Inst Health, Bethesda), DHHS Publ No (NIH) 85-23.
58. Tai C, Kuzmiski JB, MacVicar BA (2006) Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons. J Neurosci 26(23):6249-6258.