Long-term seizure suppression and optogenetic analyses of synaptic connectivity in epileptic mice with hippocampal grafts of GABAergic interneurons

Journal of Neuroscience

Volumn 34, Issue 40, 2014, Pages 13492-13504

  Henderson, Katharine W ^a   Gupta, Jyoti ^a   Tagliatela, Stephanie ^a,b   Litvina, Elizabeth ^a,c   Zheng, Xiaoting ^a   Van Zandt, Meghan A ^a   Woods, Nicholas ^a   Grund, Ethan ^a   Lin, Diana ^a   Royston, Sara ^a,d   Yanagawa, Yuchio ^e   Aaron, Gloster B ^a   Naegele, Janice R ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

EEG; Epilepsy; GABA; Seizures; Transplantation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM BINDING PROTEIN; GEPHYRIN; BACTERIAL PROTEIN; CHANNELRHODOPSIN 2, MOUSE; NERVE PROTEIN; PHOTOPROTEIN; RHODOPSIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VIAAT PROTEIN, MOUSE; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONFOCAL MICROSCOPY; CONNECTOME; CONTROLLED STUDY; DAM (ANIMAL); DENDRITE; DENTATE GYRUS; ELECTRODE IMPLANTATION; ELECTROENCEPHALOGRAPHY; EMBRYO; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MEDIAN EMINENCE; MOUSE; NERVE FIBER; NERVE GRAFT; NERVE TRANSPLANTATION; NONHUMAN; OPTOGENETICS; PROTEIN EXPRESSION; TEMPORAL LOBE EPILEPSY; VIDEORECORDING; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DISEASE MODEL; EPILEPSY; GENETICS; GENICULATE BODY; HIPPOCAMPUS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALS; BACTERIAL PROTEINS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; EPILEPSY; GABAERGIC NEURONS; GENICULATE BODIES; HIPPOCAMPUS; IN VITRO TECHNIQUES; INTERNEURONS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; RHODOPSIN; SYNAPTIC POTENTIALS; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84907494889     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0005-14.2014     Document Type: Article

References (59)

1. Alvarez-DoladoMCalcagnottoMEKarkarKMSouthwellDGJones-DavisDMEstradaRCRubensteinJLAlvarez-BuyllaABarabanSC(2006)Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain.J Neurosci26:7380-7389.CrossRef Medline
2. BarabanSCSouthwellDGEstradaRCJonesDLSebeJYAlfaro-CervelloCGarcía-VerdugoJMRubensteinJLAlvarez-BuyllaA(2009)Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice.Proc Natl Acad Sci U S A106:15472-15477.CrossRef Medline
3. BuckmasterPSDudekFE(1997)Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization.J Neurophysiol77:2685-2696.Medline
4. BuckmasterPSLewFH(2011)Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy.J Neurosci31:2337-2347.CrossRef Medline
5. BuckmasterPSWenX (2011)Rapamycin suppresses axon sprouting by somatostatin interneurons in a mouse model of temporal lobe epilepsy.Epilepsia52:2057-2064.CrossRef Medline
6. BuckmasterPSIngramEAWenX (2009)Inhibition of the mammalian target of rapamycin signaling pathway suppresses dentate granule cell axon sprouting in a rodent model of temporal lobe epilepsy.J Neurosci29:8259-8269.CrossRef Medline
7. CalcagnottoMEZipancicIPiquer-GilMMelloLEAlvarez-DoladoM(2010)Grafting of GABAergic precursors rescues deficits in hippocampal inhibition.Epilepsia51:66-70.CrossRef Medline
8. CalcagnottoMERuizLPBlancoMMSantos-JuniorJGValenteMFPattiCFrussa-FilhoRSantiagoMFZipancicIAlvarez-DoladoMMelloLELongoBM(2010)Effect of neuronal precursor cells derived from medial ganglionic eminence in an acute epileptic seizure model.Epilepsia51:71-75.CrossRef Medline
9. CarpentinoJEHartmanNWGrabelLBNaegeleJR(2008)Region-specific differentiation of embryonic stem cell-derived neural progenitor transplants into the adult mouse hippocampus following seizures.J Neurosci Res86:512-524.CrossRef Medline
10. CuriaGLongoDBiaginiGJonesRSAvoliM(2008)The pilocarpine model of temporal lobe epilepsy.J Neurosci Methods172:143-157.CrossRef Medline
11. DanzerSC(2008)Postnatal and adult neurogenesis in the development of human disease.Neuroscientist14:446-458.CrossRef Medline
12. Danzer SC He X Loepke AW McNamara JO (2010) Structural plasticity of dentate granule cell mossy fibers during the development of limbic epilepsy.Hippocampus 20:113-124.CrossRef Medline
13. de LanerolleNCKimJHRobbinsRJSpencerDD(1989)Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495:387-395.CrossRef Medline
14. de LanerolleNCKimJHWilliamsonASpencerSSZaveriHPEidTSpencerDD(2003)A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44:677-687.CrossRef Medline
15. de LanerolleNCLeeTSSpencerD(2012)Histopathology of human epilepsy. In:Jasper’s basic mechanisms of the epilepsies, Ed4(Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV).Bethesda, MD:National Center For Biotechnology Information.
16. FangMShenLYinHPanYMWangLChenDXiZQXiaoZWangXFZhouSN(2011)Downregulation of gephyrin in temporal lobe epilepsy neurons in humans and a rat model. Synapse 65:1006-1014.CrossRef Medline
17. FreundTFBuzsákiG(1996)Interneurons of the hippocampus. Hippocampus 6:347-470.Medline
18. FreundTFYlinenAMiettinenRPitkänenALahtinenHBaimbridgeKGRiekkinenPJ(1992)Pattern of neuronal death in the rat hippocampus after status epilepticus: relationship to calcium binding protein content and ischemic vulnerability. Brain Res Bull 28:27-38.CrossRef Medline
19. GermainNDBandaECBeckerSNaegeleJRGrabelLB(2013)Derivation and isolation of NKX2.1-positive basal forebrain progenitors from human embryonic stem cells. Stem Cells Dev 22:1477-1489.CrossRef Medline
20. GernertMThompsonKWLöscherWTobinAJ(2002)Genetically engineered GABA-producing cells demonstrate anticonvulsant effects and long-term transgene expression when transplanted into the central piriform cortex of rats. Exp Neurol 176:183-192.CrossRef Medline
21. GonzálezMICruz Del AngelYBrooks-KayalA(2013)Down-regulation of gephyrin and GABAA receptor subunits during epileptogenesis in the CA1 region of hippocampus. Epilepsia 54:616-624.CrossRef Medline
22. HartmanNWCarpentinoJELaMonicaKMorDENaegeleJRGrabelL(2010)CXCL12-mediated guidance of migrating embryonic stem cell-derived neural progenitors transplanted into the hippocampus. PloS One 5:e15856.CrossRef Medline
23. HouserCR(1990)Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 535:195-204.CrossRef Medline
24. HuntRFGirskisKMRubensteinJLAlvarez-BuyllaABarabanSC(2013)GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior. Nat Neurosci 16:692-697.CrossRef Medline
25. KriegsteinAAlvarez-BuyllaA(2009)The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.CrossRef Medline
26. Kumar SS, Buckmaster PS (2006)Hyperexcitability, interneuronsand loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 26:4613-4623. CrossRef Medline
27. Long L, Xiao B, Feng L, Yi F, Li G, Li S, Mutasem MA, Chen S, Bi F, Li Y (2011) Selective loss and axonal sprouting of GABAergic interneurons in the sclerotic hippocampus induced by LiCl-pilocarpine. Int J Neurosci 121:69-85. CrossRef Medline
28. MaisanoXLitvinaETagliatelaSAaronGBGrabelLBNaegeleJR(2012)Differentiation and functional incorporation of embryonic stem cell-derived GABAergic interneurons in the dentate gyrus of mice with temporal lobe epilepsy. J Neurosci 32:46-61.CrossRef Medline
29. MargerisonJHCorsellisJA(1966)Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89:499-530.CrossRef Medline
30. MaroofAMKerosSTysonJAYingSWGanatYMMerkleFTLiuBGoulburnAStanleyEGElefantyAGWidmerHREgganKGoldsteinPAAndersonSAStuderL(2013)Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12:559-572.CrossRef Medline
31. MathernGWBabbTLVickreyBGMelendezMPretoriusJK(1995)The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118:105-118.CrossRef Medline
32. MazzuferiMKumarGRospoCKaminskiRM(2012)Rapid epileptogenesis in the mouse pilocarpine model: video-EEG, pharmacokinetic and histopathological characterization. Exp Neurol 238:156-167.CrossRef Medline
33. MurphyBLPunRYYinHFaulknerCRLoepkeAWDanzerSC(2011)Heterogeneous integration of adult-generated granule cells into the epileptic brain. J Neurosci 31:105-117.CrossRef Medline
34. NadlerJV(2003)The recurrent mossy fiber pathway of the epileptic brain. Neurochem Res 28:1649-1658.CrossRef Medline
35. Nait OumesmarBVignaisLBaron-Van EvercoorenA(1997)Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. J Neurosci 17:125-139.Medline
36. NicholasCRChenJTangYSouthwellDGChalmersNVogtDArnoldCMChenYJStanleyEGElefantyAGSasaiYAlvarez-BuyllaARubensteinJLKriegsteinAR(2013)Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12:573-586.CrossRef Medline
37. Paxinos GF. Franklin KB.(2008)The mouse brain in stereotaxic coordinates Ed 3.San Diego:Academic.
38. PengZZhangNWeiWHuangCSCetinaYOtisTSHouserCR(2013)A reorganized GABAergic circuit in a model of epilepsy: evidence from optogenetic labeling and stimulation of somatostatin interneurons. J Neurosci 33:14392-14405.CrossRef Medline
39. ScharfmanHEPierceJP(2012)New insights into the role of hilar ectopic granule cells in the dentate gyrus based on quantitative anatomic analysis and three-dimensional reconstruction. Epilepsia 53:109-115.CrossRef Medline
40. ScharfmanHEGoodmanJHSollasAL(2000)Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 20:6144-6158.Medline
41. ScharfmanHESollasAEBergerREGoodmanJHPierceJP(2003)Perforant path activation of ectopic granule cells that are born after pilocarpine-induced seizures. Neuroscience 121:1017-1029.CrossRef Medline
42. SchoenenbergerPSchärerYPZOertnerTG(2011)Channelrhodopsin as a tool to investigate synaptic transmission and plasticity. Exp Physiol 96: 34-39.CrossRef Medline
43. Shibley H, Smith BN (2002) Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res 49:109-120. CrossRef Medline
44. Swartz BE, Houser CR, Tomiyasu U, Walsh GO, DeSalles A, Rich JR, Delgado-Escueta A (2006) Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia 47:1373-1382. CrossRef Medline
45. TauckDLNadlerJV(1985)Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.Medline
46. ThindKKYamawakiRPhanwarIZhangGWenXBuckmasterPS(2010)Initial loss but later excess of GABAergic synapses with dentate granule cells in a rat model of temporal lobe epilepsy. J Comp Neurol 518:647-667.CrossRef Medline
47. ThompsonK(2009)Transplantation of GABA-producing cells for seizure control in models of temporal lobe epilepsy. Neurotherapeutics 6:284-294.CrossRef Medline
48. TóthKErossLVajdaJHalászPFreundTFMaglóczkyZ(2010)Loss and reorganization of calretinin-containing interneurons in the epileptic human hippocampus. Brain 133:2763-2777.CrossRef Medline
49. TysonJAAndersonSA(2014)GABAergic interneuron transplants to study development and treat disease. Trends Neurosci 37:169-177.CrossRef Medline
50. WaldauBHattiangadyBKurubaRShettyAK(2010)Medial ganglionic eminence-derived neural stem cell grafts ease spontaneous seizures and restore GDNF expression in a rat model of chronic temporal lobe epilepsy. Stem Cells 28:1153-1164.CrossRef Medline
51. WalterCMurphyBLPunRYSpieles-EngemannALDanzerSC(2007)Pilocarpine-induced seizures cause selective time-dependent changes to adult-generated hippocampal dentate granule cells. J Neurosci 27:7541-7552.CrossRef Medline
52. WangHPecaJMatsuzakiMMatsuzakiKNoguchiJQiuLWangDZhangFBoydenEDeisserothKKasaiHHallWCFengGAugustineGJ(2007)High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci U S A 104:8143-8148.CrossRef Medline
53. WangYKakizakiTSakagamiHSaitoKEbiharaSKatoMHirabayashiMSaitoYFuruyaNYanagawaY(2009)Fluorescent labeling of both GABAaergic and glycinergic neurons in vesicular GABA transporter (VGAT)-Venus transgenic mouse. Neuroscience 164:1031-1043.CrossRef Medline
54. WichterleHGarcia-VerdugoJMHerreraDGAlvarez-BuyllaA(1999)Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2:461-466.CrossRef Medline
55. WoodruffRHTekki-KessarisNStilesCDRowitchDHRichardsonWD(2001)Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives.Int J Dev Neurosci 19:379-385.CrossRef Medline
56. XuQCobosIDe La CruzERubensteinJLAndersonSA(2004)Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.CrossRef Medline
57. ZhangWYamawakiRWenXUhlJDiazJPrinceDABuckmasterPS(2009)Surviving hilar somatostatin interneurons enlarge, sprout axons, and form new synapses with granule cells in a mouse model of temporal lobe epilepsy. J Neurosci 29:14247-14256.CrossRef Medline
58. ZhaoSTingJTAtallahHEQiuLTanJGlossBAugustineGJDeisserothKLuoMGraybielAMFengG(2011)Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat Methods 8:745-752.CrossRef Medline
59. ZipancicICalcagnottoMEPiquer-GilMMelloLEAlvarez-DoladoM(2010)Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility. Cell Transplantation 19:549-564.CrossRef Medline