An epilepsy-related ARX polyalanine expansion modifies glutamatergic neurons excitability and morphology without affecting gabaergic neurons development

Cerebral Cortex

Volumn 23, Issue 6, 2013, Pages 1484-1494

  Beguin, Shirley ^a,b   Crépel, Valérie ^a,b   Aniksztejn, Laurent ^a,b   Becq, Hélène ^a,b   Pelosi, Barbara ^c   Pallesi Pocachard, Emilie ^a,b   Bouamrane, Lamine ^a,b   Pasqualetti, Massimo ^c   Kitamura, Kunio ^d   Cardoso, Carlos ^a,b   Represa, Alfonso ^a,b  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITY OF PISA   (Italy)

^d NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

ARX; epilepsy; network excitability; neuronal migration

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARISTALESS RELATED HOMEOBOX GENE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; EPILEPSY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABA NEURON; GENE MUTATION; GENE TARGETING; GENETIC ANALYSIS; GENOME; HIPPOCAMPUS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE FIBER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; WILD TYPE;

ARX; EPILEPSY; NETWORK EXCITABILITY; NEURONAL MIGRATION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELL MOVEMENT; ELECTROPORATION; EMBRYO, MAMMALIAN; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; GLUTAMATES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; LYSINE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PEPTIDES; RNA, SMALL INTERFERING; STATISTICS, NONPARAMETRIC; SYNAPTIC POTENTIALS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84877268023     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs138     Document Type: Article

References (32)

1. Absoud M, Parr JR, Halliday D, Pretorius P, Zaiwalla Z, Jayawant S. 2010. A novel ARX phenotype: rapid neurodegeneration with Oh-tahara syndrome and a dyskinetic movement disorder. Dev Med Child Neurol. 52:305-307.
2. Ackman JB, Aniksztejn L, Crépel V, Becq H, Pellegrino C, Cardoso C, Ben-Ari Y, Represa A. 2009. Abnormal network activity in a targeted genetic model of human double cortex. J Neurosci. 29:313-327.
3. Aniksztejn L, Demarque M, Morozov Y, Ben-Ari Y, Represa A. 2001. Recurrent CA1 collateral axons in developing rat hippocampus. Brain Res. 913:195-200.
4. Bienvenu T, Poirier K, Friocourt G, Bahi N, Beaumont D, Fauchereau F, Ben Jeema L, Zemni R, Vinet MC, Francis F et al. 2002. ARX, a novel Prd-class-homeobox gene highly expressed in the telence-phalon, is mutated in X-linked mental retardation. Hum Mol Genet. 11:981-991.
5. Colombo E, Collombat P, Colasante G, Bianchi M, Long J, Mansouri A, Rubenstein JL, Broccoli V. 2007. Inactivation of Arx, the murine ortholog of the X-linked lissencephaly with ambiguous genitalia gene, leads to severe disorganization of the ventral telencephalon with impaired neuronal migration and differentiation. J Neurosci. 27:4786-4798.
6. Colombo E, Galli R, Cossu G, Gecz J, Broccoli V. 2004. Mouse ortholo-gue of ARX, a gene mutated in several X-linked forms of mental retardation and epilepsy, is a marker of adult neural stem cells and forebrain GABAergic neurons. Dev Dyn. 231:631-639.
7. Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C. 1999. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol. 408:449-460.
8. Frankel WN. 2009. Genetics of complex neurological disease: challenges and opportunities for modeling epilepsy in mice and rats. Trends Genet. 25:361-367.
9. Friocourt G, Kanatani S, Tabata H, Yozu M, Takahashi T, Antypa M, Raguénès O, Chelly J, Férec C, Nakajima K et al. 2008. Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J Neurosci. 28:5794-5805.
10. Friocourt G, Poirier K, Rakic S, Parnavelas JG, Chelly J. 2006. The role of ARX in cortical development. Eur J Neurosci. 23:869-876.
11. Gecz J, Cloosterman D, Partington M. 2006. ARX: a gene for all seasons. Curr Opin Genet Dev. 16:308-316.
12. Gelman DM, Marín O. 2010. Generation of interneuron diversity in the mouse cerebral cortex. Eur J Neurosci. 31:2136-2141.
13. Guerrini R, Moro F, Kato M, Barkovich AJ, Shiihara T, McShane MA, Hurst J, Loi M, Tohyama J, Norci V et al. 2007. Expansion of the first polyA tract of ARX causes infantile spasms and status dystoni-cus. Neurology. 69:427-433.
14. Huberfeld G, Menendez de la Prida L, Pallud J, Cohen I, Le Van Quyen M, Adam C, Clemenceau S, Baulac M, Miles R. 2011. Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy. Nat Neurosci. 14:627-634.
15. Kato M, Das S, Petras K, Kitamura K, Morohashi K, Abuelo DN, Barr M, Bonneau D, Brady AF, Carpenter NJ. 2004. Mutations of ARX are associated with striking pleiotropy and consistent genotype-phenotype correlation. Hum Mutat. 23:147-159.
16. Kato M, Dobyns WB. 2005. X-linked lissencephaly with abnormal genitalia as a tangential migration disorder causing intractable epilepsy: proposal for a new term, "interneuronopathy." J Child Neurol. 20:392-397.
17. Kitamura K, Itou Y, Yanazawa M, Ohsawa M, Suzuki-Migishima R, Umeki Y, Hohjoh H, Yanagawa Y, Shinba T, Itoh M et al. 2009 Three human ARX mutations cause the lissencephaly-like and mental retardation with epilepsy-like pleiotropic phenotypes in mice. Hum Mol Genet. 18:3708-3724.
18. Kitamura K, Yanazawa M, Sugiyama N, Miura H, Iizuka-Kogo A, Kusaka M, Omichi K, Suzuki R, Kato-Fukui Y, Kamiirisa K. 2002. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat Genet. 32:359-369.
19. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science. 321:53-57.
20. Korff CM, Nordli DRJ. 2006. Epilepsy syndromes in infancy. Pediatr Neurol. 34:253-263.
21. Lehmann TN, Gabriel S, Kovacs R, Eilers A, Kivi A, Schulze K, Lanksch WR, Meencke HJ, Heinemann U. 2000. Alterations of neuronal connectivity in area CA1 of hippocampal slices from temporal lobe epilepsy patients and from pilocarpine-treated epileptic rats. Epilepsia. 41(Suppl. 6):S190-S194.
22. Liotta A, Caliskan G, ul Haq R, Hollnagel JO, Rösler A, Heinemann U, Behrens CJ. 2011. Partial disinhibition is required for transition of stimulus-induced sharp wave-ripple complexes into recurrent epileptiform discharges in rat hippocampal slices. J Neurophysiol. 105:172-187.
23. Marcorelles P, Laquerriere A, Adde-Michel C, Marret S, Saugier-Veber P, Beldjord C, Friocourt G. 2010. Evidence for tangential migration disturbances in human lissencephaly resulting from a defect in LIS1, DCX and ARX genes. Acta Neuropathol. 120:503-515.
24. Nabbout R, Dulac O. 2008. Epileptic syndromes in infancy and childhood. Curr Opin Neurol. 21:161-166.
25. Nasrallah MP, Cho G, Putt ME, Kitamura K, Golden JA. 2011. Differential effects of a polyalanine tract expansion in Arx on neural development and gene expression. Hum Mol Genet. 21:1090-1098.
26. Okazaki S, Ohsawa M, Kuki I, Kawawaki H, Koriyama T, Ri S, Ichiba H, Hai E, Inoue T, Nakamura H. 2008. Aristaless-related homeo-box gene disruption leads to abnormal distribution of GABAergic interneurons in human neocortex: evidence based on a case of X-linked lissencephaly with abnormal genitalia (XLAG). Acta Neuropathol. 116:453-462.
27. Poirier K, Van Esch H, Friocourt G, Saillour Y, Bahi N, Backer S, Souil E, Castelnau-Ptakhine L, Beldjord C, Francis F. 2004. Neuroanato-mical distribution of ARX in brain and its localisation in GABAergic neurons. Brain Res Mol Brain Res. 122:35-46.
28. Price MG, Yoo JW, Burgess DL, Deng F, Hrachovy RA, Frost JD Jr, Noebels JL. 2009. A triplet repeat expansion genetic mouse model of infantile spasms syndrome, Arx(GCG)10+7, with interneuronopathy, spasms in infancy, persistent seizures, and adult cognitive and behavioral impairment. J Neurosci. 29:8752-8763.
29. Represa A, Ben-Ari Y. 2005. Trophic actions of GABA on neuronal development. Trends Neurosci. 28:278-283.
30. Shoubridge C, Cloosterman D, Parkinson-Lawerence E, Brooks D, Gecz J. 2007. Molecular pathology of expanded polyalanine tract mutations in the Aristaless-related homeobox gene. Genomics. 90:59-71.
31. Shoubridge C, Fullston T, Gecz J. 2010. ARX spectrum disorders: making inroads into the molecular pathology. Hum Mutat. 31:889-900.
32. Stromme P, Mangelsdorf ME, Scheffer IE, Gecz J. 2002. Infantile spasms, dystonia, and other X-linked phenotypes caused by mutations in Aristaless related homeobox gene, ARX. Brain Dev. 24:266-268.