GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior

Nature Neuroscience

Volumn 16, Issue 6, 2013, Pages 692-697

  Hunt, Robert F ^a,b   Girskis, Kelly M ^a,b   Rubenstein, John L ^a   Alvarez Buylla, Arturo ^b   Baraban, Scott C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CALRETININ; NITRIC OXIDE SYNTHASE; PARVALBUMIN; SOMATOSTATIN;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CELL MIGRATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EPILEPSY; HIPPOCAMPUS; HYPERACTIVITY; INTERNEURON; MALE; MOTOR COORDINATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE GRAFT; NERVE TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITY OF LIFE; SEIZURE; SHORT TERM MEMORY; SPATIAL LEARNING; SYNAPTIC TRANSMISSION;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY; EPILEPSY, TEMPORAL LOBE; GABAERGIC NEURONS; INTERNEURONS; MICE; STEM CELL TRANSPLANTATION; TELENCEPHALON;

EID: 84878531145     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3392     Document Type: Article

References (42)

1. Lothman, E.W., Bertram, E.H. III & Stringer, J.L. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37, 1-82 (1991)
2. Noebels, J.L., Avoli, M., Rogawski, M.A., Olsen, R.W. & Delgado-Escueta, A.V. Jasper's Basic Mechanisms of the Epilepsies, 4th edn. (National Center for Biotechnology, Bethesda, Maryland, 2012)
3. Andrews-Zwilling, Y. et al. Hilar GABAergic interneuron activity controls spatial learning and memory retrieval. PLoS ONE 7, e40555 (2012)
4. Han, S. et al. Autistic-like behavior in Scn1a+/ mice and rescue by enhanced GABA-mediated neurotransmission. Nature 489, 385-390 (2012)
5. Anonymous. Epilepsy Fact Sheet. World Health Organization 〈http://www.who.int/mediacentre/factsheets/fs999/en/index.html〉 (October 2012)
6. Paz, J.T. et al. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 16, 64-70 (2013)
7. Krook-Magnuson, E., Armstrong, C., Oijala, M. & Soltesz, I. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat. Commun. 4, 1376 (2013)
8. Lavdas, A.A., Grigoriou, M., Pachnis, V. & Parnavelas, J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888 (1999)
9. Wichterle, H., Garcia-Verdugo, J.M., Herrera, D.G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461-466 (1999)
10. Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J.L. & Anderson, S.A. Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622 (2004)
11. Butt, S.J. et al. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48, 591-604 (2005)
12. Alvarez-Dolado, M. et al. Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J. Neurosci. 26, 7380-7389 (2006)
13. Baraban, S.C. et al. Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice. Proc. Natl. Acad. Sci. USA 106, 15472-15477 (2009)
14. Southwell, D.G. et al. Intrinsically determined cell death of developing cortical interneurons. Nature 491, 109-113 (2012)
15. Shibley, H. & Smith, B.N. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 49, 109-120 (2002)
16. Goffin, K., Nissinen, J., Van Laere, K. & Pitkänen, A. Cyclicity of spontaneous recurrent seizures in pilocarpine model of temporal lobe epilepsy in rat. Exp. Neurol. 205, 501-505 (2007)
17. Bortel, A., Lévesque, M., Biagini, G., Gotman, J. & Avoli, M. Convulsive status epilepticus duration as determinant for epileptogenesis and interictal discharge generation in the rat limbic system. Neurobiol. Dis. 40, 478-489 (2010)
18. Gröticke, I., Hoffmann, K. & Löscher, W. Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp. Neurol. 207, 329-349 (2007)
19. Löscher, W. Strategies for antiepileptogenesis: antiepileptic drugs versus novel approaches evaluated in post-status epilepticus models of temporal lobe epilepsy. in Jasper's Basic Mechanisms of the Epilepsies, 4th edn. (eds. Noebels, J.L., Avoli, M., Rogawski, M.A., Olsen, R.W. & Delgado-Escueta, A.V.) (National Center for Biotechnology Information, Bethesda, Maryland, 2012)
20. Hadjantonakis, A., Gertenstein, M., Ikawa, M., Okabe, M. & Nagy, A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 76, 79-90 (1998)
21. Tricoire, L. et al. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J. Neurosci. 31, 10948-10970 (2011)
22. Vignoli, T. et al. Consequences of pilocarpine-induced status epilepticus in immunodeficient mice. Brain Res. 1450, 125-137 (2012)
23. Racine, R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294 (1972)
24. Babb, T.L., Kupfer, W.R., Pretorius, J.K., Crandall, P.H. & Levesque, M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42, 351-363 (1991
25. Palmiter, R.D., Cole, T.B., Quaife, C.J. & Findley, S.D. ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc. Natl. Acad. Sci. USA 93, 14934-14939 (1996)
26. Hermann, B., Seidenberg, M. & Jones, J. The neurobehavioural comorbidities of epilepsy: can a natural history be developed. Lancet Neurol. 7, 151-160 (2008)
27. D'Hooge, R. & De Deyn, P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 36, 60-90 (2001)
28. Palop, J.J. et al. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc. Natl. Acad. Sci. USA 100, 9572-9577 (2003)
29. Verret, L. et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149, 708-721 (2012)
30. Hirsch, J.C. et al. Deficit of quantal release of GABA in experimental models of temporal lobe epilepsy. Nat. Neurosci. 2, 499-500 (1999)
31. Cossart, R. et al. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4, 52-62 (2001)
32. Kobayashi, M. & Buckmaster, P.S. Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J. Neurosci. 23, 2440-2452 (2003)
33. Zipancic, I., Calcagnotto, M.E., Piquer-Gil, M., Mello, L.E. & Alvarez-Dolado, M. Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility. Cell Transplant. 19, 549-564 (2010)
34. Chagnac-Amitai, Y. & Connors, B.W. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747-758 (1989)
35. Trevelyan, A.J., Sussillo, D. & Yuste, R.M. Feedforward inhibition contributes to the control of the speed of epileptiform propagation. J. Neurosci. 27, 3383-3387 (2007)
36. Schevon, C.A. et al. Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun. 3, 1060 (2012)
37. Berényi, A., Belluscio, M., Mao, D. & Buzsaki, G. Closed-loop control of epilepsy by transcranial electrical stimulation. Science 337, 735-737 (2012)
38. Marchenko, S. & Flanagan, L. Counting human neural stem cells. J. Vis. Exp. 7, 262 (2007)
39. Vucurovic, K. et al. Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb. Cortex 20, 2333-2347 (2010)
40. Mortazavi, F., Ericson, M., Story, D., Hulce, V.D. & Dunbar, G.L. Spatial learning deficits and emotional impairments in pentylenetetrazole- kindled rats. Epilepsy Behav. 7, 629-638 (2005)
41. Raber, J., Bongers, G., LeFevour, A., Buttini, M. & Mucke, L. Androgens protect against apilipoprotein E4-induced cognitive deficits. J. Neurosci. 22, 5204-5209 (2002)
42. Can, A. et al. The mouse forced swim test. J. Vis. Exp. 59, 3638 (2012)