Impaired action potential initiation in GABAergic interneurons causes hyperexcitable networks in an epileptic mouse model carrying a human Nav1.1 mutation

Journal of Neuroscience

Volumn 34, Issue 45, 2014, Pages 14874-14889

  Hedrich, Ulrike B S ^a   Liautard, Camille ^b,c   Kirschenbaum, Daniel ^a   Pofahl, Martin ^d,e   Lavigne, Jennifer ^b,c   Liu, Yuanyuan ^a   Theiss, Stephan ^f,g   Slotta, Johannes ^f,g   Escayg, Andrew ^h   Dihné, Marcel ^a   Beck, Heinz ^d,e   Mantegazza, Massimo ^b,c   Lerche, Holger ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Laboratory of Excellence Ion Channel Science and Therapeutics   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d UNIVERSITY HOSPITAL BONN   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^f HEINRICH HEINE UNIVERSITY   (Germany)

^g RESULT Medical   (Germany)

^h EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epilepsy; Genetics; Ion channel; Mouse model; Network activity

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4', 6 DIAMIDINO 2 PHENYLINDOLE; CD8 ANTIGEN; ENHANCED GREEN FLUORESCENT PROTEIN; MONOCLONAL ANTIBODY; PICROTOXIN; SODIUM CHANNEL NAV1.1; UNCLASSIFIED DRUG; CALCIUM; SCN1A PROTEIN, HUMAN;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL CULTURE; CONTROLLED STUDY; EPILEPSY; FEMALE; GABAERGIC SYSTEM; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HIGH FREQUENCY OSCILLATION; HIPPOCAMPAL CA1 REGION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE FIBER MEMBRANE POTENTIAL; NERVE STIMULATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PYRAMIDAL NERVE CELL; SITE DIRECTED MUTAGENESIS; SODIUM CHANNEL NAV1.1 GENE; SODIUM CURRENT; SPIKE WAVE; STRATUM PYRAMIDALE; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; VOLTAGE CLAMP TECHNIQUE; WHOLE CELL PATCH CLAMP; ANIMAL; BRAIN; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; MUTATION; NERVE FIBER; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; AXONS; BRAIN; CALCIUM; CELLS, CULTURED; EPILEPSY; GABAERGIC NEURONS; HUMANS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MICE; MICE, INBRED C57BL; MUTATION; NAV1.1 VOLTAGE-GATED SODIUM CHANNEL; NERVE NET;

EID: 84908537805     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0721-14.2014     Document Type: Article

References (67)

1. Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365-379. CrossRef Medline
2. Alekov A, Rahman MM, Mitrovic N, Lehmann-Horn F, Lerche H (2000) A sodium channel mutation causing epilepsy in man exhibits subtle defects in fast inactivation and activation in vitro. J Physiol 529:533-539. CrossRef Medline
3. Allène C, Cattani A, Ackman JB, Bonifazi P, Aniksztejn L, Ben-Ari Y, Cossart R (2008) Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J Neurosci 28:12851-12863. CrossRef Medline
4. Baulac S, Gourfinkel-An I, Picard F, Rosenberg-Bourgin M, Prud’homme J-F, Baulac M, Brice A, LeGuern E (1999) A second locus for familial generalized epilepsy with febrile seizures plus maps to chromosome 2q21-q33. J Hum Genet 65:1078-1085.CrossRef
5. Beenhakker MP, Huguenard JR (2009) Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 62:612-632. CrossRef Medline
6. Behrens CJ, van den Boom LP, Heinemann U (2007) Effects of the GABAA receptor antagonists bicuculline and gabazine on stimulus-induced sharp wave-ripple complexes in adult rat hippocampus in vitro. Eur J Neurosci 25:2170-2181. CrossRef Medline
7. Ben-Ari Y, Dudek FE (2010) Primary and secondary mechanisms of epileptogenesis in the temporal lobe: there is a before and an after. Epilepsy Curr 10:118-125. CrossRef Medline
8. Bragin A, Mody I, Wilson CL, Engel J Jr (2002) Local generation of fast ripples in epileptic brain. J Neurosci 22:2012-2021.Medline
9. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510. CrossRef Medline
10. +channel. J Neurosci 28:7273-7283. CrossRef Medline
11. Christian CA, Herbert AG, Holt RL, Peng K, Sherwood KD, Pangratz-Fuehrer S, Rudolph U, Huguenard JR (2013) Endogenous positive allosteric modulation of GABA(A) receptors by diazepam binding inhibitor. Neuron 78:1063-1074. CrossRef Medline
12. Claes L, Del-Favero J, Ceulemans B, Lagae L, Van Broeckhoven C, De Jonghe P (2001) De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy. J Hum Genet 68:1327-1332.CrossRef
13. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78. CrossRef Medline
14. Contreras D, Curró Dossi R, Steriade M (1992) Bursting and tonic discharges in two classes of reticular thalamic neurons. J Neurophysiol 68: 973-977.Medline
15. Cope DW, Di Giovanni G, Fyson SJ, Orbán G, Errington AC, Lorincz ML, Gould TM, Carter DA, Crunelli V (2009) Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat Med 15:1392-1398. CrossRef Medline
16. Danober L, Deransart C, Depaulis A, Vergnes M, Marescaux C (1998) Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55:27-57. CrossRef Medline
17. Dichgans M, Freilinger T, Eckstein G, Babini E, Lorenz-Depiereux B, Biskup S, Ferrari MD, Herzog J, van den Maagdenberg AM, Pusch M, Strom TM (2005) Mutation in the neuronal voltage-gated sodium channel SCN1A in familial hemiplegic migraine. Lancet 366:371-377. CrossRef Medline
18. Dutton SB, Makinson CD, Papale LA, Shankar A, Balakrishnan B, Nakazawa K, Escayg A (2012) Preferential inactivation of Scn1a in parvalbumin interneurons increases seizure susceptibility. Neurobiol Dis 49C:211-220. CrossRef Medline
19. 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 (2000) Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat Genet 24:343-345. CrossRef Medline
20. Glasscock E, Qian J, Yoo JW, Noebels JL (2007) Masking epilepsy by combining two epilepsy genes. Nat Neurosci 10:1554-1558. CrossRef Medline
21. Grewe BF, Langer D, Kasper H, Kampa BM, Helmchen F (2010) High-speed in vivo calcium imaging reveals neuronal network activity with nearmillisecond precision. Nat Methods 7:399-405. CrossRef Medline
22. Henze DA, González-Burgos GR, Urban NN, Lewis DA, Barrionuevo G (2000) Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84:2799-2809.Medline
23. Holekamp TF, Turaga D, Holy TE (2008) Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57:661-672. CrossRef Medline
24. +channels ensures fast signaling in GABAergic interneuron axons. Nat Neurosci 17:686-693. CrossRef Medline
25. Hu H, Martina M, Jonas P (2010) Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science 327:52-58. CrossRef Medline
26. Huntsman MM, Porcello DM, Homanics GE, DeLorey TM, Huguenard JR (1999) Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 283:541-543. CrossRef Medline
27. Illes S, Theiss S, Hartung HP, Siebler M, Dihne´ M (2009) Niche-dependent development of functional neuronal networks from embryonic stem cellderived neural populations. BMC Neurosci 10:93. CrossRef Medline
28. Jefferys JG, Menendez delaPrida L, Wendling F, Bragin A, Avoli M, Timofeev I, Lopes da Silva FH (2012) Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol 98:250-264. CrossRef Medline
29. Jia F, Pignataro L, Schofield CM, Yue M, Harrison NL, Goldstein PA (2005) An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons. J Neurophysiol 94:4491-4501. CrossRef Medline
30. Jones MS, Barth DS (2002) Effects of bicuculline methiodide on fast (>200 Hz) electrical oscillations in rat somatosensory cortex. J Neurophysiol 88:1016-1025.Medline
31. Korn SJ, Giacchino JL, Chamberlin NL, Dingledine R (1987) Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. J Neurophysiol 57:325-340.Medline
32. Lauxmann S, Boutry-Kryza N, Rivier C, Mueller S, Hedrich UB, Maljevic S, Szepetowski P, Lerche H, Lesca G (2013) An SCN2A mutation in a family with infantile seizures from Madagascar reveals an increased subthreshold Na current. Epilepsia 54:e117-e121. CrossRef Medline
33. Lee SH, Govindaiah G, Cox CL (2007) Heterogeneity of firing properties among rat thalamic reticular nucleus neurons. J Physiol 582:195-208. CrossRef Medline
34. Le Magueresse C, Monyer H (2013) GABAergic interneurons shape the functional maturation of the cortex. Neuron 77:388-405. CrossRef Medline
35. Liao Y, Anttonen AK, Liukkonen E, Gaily E, Maljevic S, Schubert S, Bellan-Koch A, Petrou S, Ahonen VE, Lerche H, Lehesjoki AE (2010) SCN2A mutation associated with neonatal epilepsy, late-onset episodic ataxia, myoclonus, and pain. Neurology 75:1454-1458. CrossRef Medline
36. Liautard C, Scalmani P, Carriero G, de Curtis M, Franceschetti S, Mantegazza M (2013) Hippocampal hyperexcitability and specific epileptiform activity in a mouse model of Dravet syndrome. Epilepsia 54:1251-1261. CrossRef Medline
37. Llinás RR, Steriade M (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95:3297-3308. CrossRef Medline
38. Lorincz A, Nusser Z (2008) Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28:14329-14340. CrossRef Medline
39. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884. CrossRef Medline
40. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH, Nicoud JF, Zemelman BV, Sternson SM, Losonczy A (2012) Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15: 423-430, S1-S3. CrossRef Medline
41. +channelopathies and epilepsy: recent advances and new perspectives. Expert Rev Clin Pharmacol 3:371-384. CrossRef Medline
42. +channel gating between fast-spiking interneurones and principal neurones of rat hippocampus. J Physiol 505:593-603. CrossRef Medline
43. Martina M, Vida I, Jonas P (2000) Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287:295-300. CrossRef Medline
44. Martin MS, Tang B, Papale LA, Yu FH, Catterall WA, Escayg A (2007) The voltage-gated sodium channel Scn8a is a genetic modifier of severe myoclonic epilepsy of infancy. Hum Mol Genet 16:2892-2899. CrossRef Medline
45. 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 (2010) Altered function of the SCN1A voltage-gated sodium channel leads to-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J Biol Chem 285:9823-9834. CrossRef Medline
46. Meeks JP, Mennerick S (2007) Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97:3460-3472. CrossRef Medline
47. Mistry AM, Thompson CH, Miller AR, Vanoye CG, George AL Jr, Kearney JA (2014) Strain-and age-dependent hippocampal neuron sodium currents correlate with epilepsy severity in Dravet syndrome mice. Neurobiol Dis 65:1-11. CrossRef Medline
48. 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. J Neurosci 27:5903-5914. CrossRef Medline
49. 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 seizureassociated sudden death in a mouse model of Dravet syndrome.HumMol Genet 22:4784-4804. CrossRef Medline
50. Palmer LM, Stuart GJ (2006) Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26:1854-1863. CrossRef Medline
51. Rasband MN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552-562. CrossRef Medline
52. Redecker C, Luhmann HJ, Hagemann G, Fritschy JM, Witte OW (2000) Differential downregulation of GABAA receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J Neurosci 20:5045-5053.Medline
53. Reid CA, Berkovic SF, Petrou S (2009) Mechanisms of human inherited epilepsies. Prog Neurobiol 87:41-57. CrossRef Medline
54. Royeck M, Horstmann MT, Remy S, Reitze M, Yaari Y, Beck H (2008) Role of axonal NaV1.6 sodium channels in action potential initiation of CA1 pyramidal neurons. J Neurophysiol 100:2361-2380. CrossRef Medline
55. +channel mutant. J Neurosci 27:11037-11046. CrossRef Medline
56. Scheffer IE, Berkovic SF (1997) Generalized epilepsy with febrile seizures plus. A genetic disorder with heterogeneous clinical phenotypes. Brain 120:479-490. CrossRef Medline
57. Schock SC, Jolin-Dahel KS, Schock PC, Theiss S, Arbuthnott GW, Garcia-Munoz M, Staines WA (2012) Development of dissociated cryopreserved rat cortical neurons in vitro. J Neurosci Methods 205:324-333. CrossRef Medline
58. Spampanato J, Escayg A, Meisler MH, Goldin AL (2001) Functional effects of two voltage-gated sodium channel mutations that cause generalized epilepsy with febrile seizures plus type 2. J Neurosci 21:7481-7490.Medline
59. Steriade M (2005) Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 28:317-324. CrossRef Medline
60. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, 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. CrossRef Medline
61. Tang B, Dutt K, Papale L, Rusconi R, Shankar A, Hunter J, Tufik S, Yu FH, Catterall WA, Mantegazza M, Goldin AL, Escayg A (2009) A BAC transgenic mouse model reveals neuron subtype-specific effects of a Generalized Epilepsy with Febrile Seizures Plus (GEFS_) mutation. Neurobiol Dis 35:91-102. CrossRef Medline
62. Van Wart A, Trimmer JS, Matthews G (2007) Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 500:339-352. CrossRef Medline
63. Weber YG, Lerche H (2008) Genetic mechanisms in idiopathic epilepsies. Dev Med Child Neurol 50:648-654. CrossRef Medline
64. Wimmer VC, Reid CA, Mitchell S, Richards KL, Scaf BB, Leaw BT, Hill EL, Royeck M, Horstmann MT, Cromer BA, Davies PJ, Xu R, Lerche H, Berkovic SF, Beck H, Petrou S (2010) Axon initial segment dysfunction in a mouse model of genetic epilepsy with febrile seizures plus. J Clin Invest 120:2661-2671. CrossRef Medline
65. Woolson R, Clarke W (2002) Statistical methods for the analysis of biomedical data, Ed 2. New York: Wiley-Interscience.
66. 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. Nat Neurosci 9:1142-1149. CrossRef Medline
67. Zuberi SM, Brunklaus A, Birch R, Reavey E, Duncan J, Forbes GH (2011) Genotype-phenotype associations in SCN1A-related epilepsies. Neurology 76:594-600. CrossRef Medline