Cellular and Molecular Neurobiology

, Volume 30, Issue 2, pp 199–218

Neural Stem/Progenitor Cells Derived from the Embryonic Dorsal Telencephalon of D6/GFP Mice Differentiate Primarily into Neurons After Transplantation into a Cortical Lesion

  • Iva Prajerova
  • Pavel Honsa
  • Alexandr Chvatal
  • Miroslava Anderova
Original Research


D6 is a promoter/enhancer of the mDach1 gene that is involved in the development of the neocortex and hippocampus. It is expressed by proliferating neural stem/progenitor cells (NSPCs) of the cortex at early stages of neurogenesis. The differentiation potential of NSPCs isolated from embryonic day 12 mouse embryos, in which the expression of green fluorescent protein (GFP) is driven by the D6 promoter/enhancer, has been studied in vitro and after transplantation into the intact adult rat brain as well as into the site of a photochemical lesion. The electrophysiological properties of D6/GFP-derived cells were studied using the whole-cell patch-clamp technique, and immunohistochemical analyses were carried out. D6/GFP-derived neurospheres expressed markers of radial glia and gave rise predominantly to immature neurons and GFAP-positive cells during in vitro differentiation. One week after transplantation into the intact brain or into the site of a photochemical lesion, transplanted cells expressed only neuronal markers. D6/GFP-derived neurons were characterised by the expression of tetrodotoxin-sensitive Na+-currents and KA- and KDR currents sensitive to 4-aminopyridine. They were able to fire repetitive action potentials and responded to the application of GABA. Our results indicate that after transplantation into the site of a photochemical lesion, D6/GFP-derived NSPCs survive and differentiate into neurons, and their membrane properties are comparable to those transplanted into the non-injured cortex. Therefore, region-specific D6/GFP-derived NSPCs represent a promising tool for studying neurogenesis and cell replacement in a damaged cellular environment.


Ischemia Ion channels Patch-clamp Injury and repair 

Supplementary material

10571_2009_9443_MOESM1_ESM.doc (26 kb)
(DOC 26 kb)
10571_2009_9443_MOESM2_ESM.pdf (178 kb)
(PDF 177 kb)


  1. Abematsu M, Kagawa T, Fukuda S, Inoue T, Takebayashi H, Komiya S, Taga T (2006) Basic fibroblast growth factor endows dorsal telencephalic neural progenitors with the ability to differentiate into oligodendrocytes but not gamma-aminobutyric acidergic neurons. J Neurosci Res 83(5):731–743CrossRefPubMedGoogle Scholar
  2. Akesson E, Piao JH, Samuelsson EB, Holmberg L, Kjaeldgaard A, Falci S, Sundstrom E, Seiger A (2007) Long-term culture and neuronal survival after intraspinal transplantation of human spinal cord-derived neurospheres. Physiol Behav 92(1–2):60–66CrossRefPubMedGoogle Scholar
  3. Anderova M, Antonova T, Petrik D, Neprasova H, Chvatal A, Sykova E (2004) Voltage-dependent potassium currents in hypertrophied rat astrocytes after a cortical stab wound. Glia 48(4):311–326CrossRefPubMedGoogle Scholar
  4. Anderova M, Kubinova S, Jelitai M, Neprasova H, Glogarova K, Prajerova I, Urdzikova L, Chvatal A, Sykova E (2006) Transplantation of embryonic neuroectodermal progenitor cells into the site of a photochemical lesion: immunohistochemical and electrophysiological analysis. J Neurobiol 66(10):1084–1100CrossRefPubMedGoogle Scholar
  5. Andreasen M, Skov J, Nedergaard S (2007) Inwardly rectifying K(+) (Kir) channels antagonize ictal-like epileptiform activity in area CA1 of the rat hippocampus. Hippocampus 17(11):1037–1048CrossRefPubMedGoogle Scholar
  6. Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19(9):1028–1033CrossRefPubMedGoogle Scholar
  7. Bai J, Ramos RL, Ackman JB, Thomas AM, Lee RV, LoTurco JJ (2003) RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat Neurosci 6(12):1277–1283CrossRefPubMedGoogle Scholar
  8. Barry PH (1994) JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51(1):107–116CrossRefPubMedGoogle Scholar
  9. Basak O, Taylor V (2007) Identification of self-replicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci 25(4):1006–1022CrossRefPubMedGoogle Scholar
  10. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 14(3 Pt 1):1030–1037PubMedGoogle Scholar
  11. Buhnemann C, Scholz A, Bernreuther C, Malik CY, Braun H, Schachner M, Reymann KG, Dihne M (2006) Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain 129(Pt 12):3238–3248CrossRefPubMedGoogle Scholar
  12. Cancedda L, Fiumelli H, Chen K, Poo MM (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27(19):5224–5235CrossRefPubMedGoogle Scholar
  13. Carletti B, Grimaldi P, Magrassi L, Rossi F (2004) Engraftment and differentiation of neocortical progenitor cells transplanted to the embryonic brain in utero. J Neurocytol 33(3):309–319CrossRefPubMedGoogle Scholar
  14. Chan-Ling T, Chu Y, Baxter L, Weible Ii M, Hughes S (2009) In vivo characterization of astrocyte precursor cells (APCs) and astrocytes in developing rat retinae: differentiation, proliferation, and apoptosis. Glia 57(1):39–53CrossRefPubMedGoogle Scholar
  15. Darsalia V, Kallur T, Kokaia Z (2007) Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur J Neurosci 26(3):605–614CrossRefPubMedGoogle Scholar
  16. Dromard C, Bartolami S, Deleyrolle L, Takebayashi H, Ripoll C, Simonneau L, Prome S, Puech S, Tran VB, Duperray C, Valmier J, Privat A, Hugnot JP (2007) NG2 and Olig2 expression provides evidence for phenotypic deregulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells 25(2):340–353CrossRefPubMedGoogle Scholar
  17. Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, Nishiyama A, Muguruma K, Sasai Y (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3(5):519–532CrossRefPubMedGoogle Scholar
  18. Englund U, Fricker-Gates RA, Lundberg C, Bjorklund A, Wictorin K (2002) Transplantation of human neural progenitor cells into the neonatal rat brain: extensive migration and differentiation with long-distance axonal projections. Exp Neurol 173(1):1–21CrossRefPubMedGoogle Scholar
  19. Eriksson C, Bjorklund A, Wictorin K (2003) Neuronal differentiation following transplantation of expanded mouse neurosphere cultures derived from different embryonic forebrain regions. Exp Neurol 184(2):615–635CrossRefPubMedGoogle Scholar
  20. Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, Sun YE (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132(15):3345–3356CrossRefPubMedGoogle Scholar
  21. Friocourt G, Liu JS, Antypa M, Rakic S, Walsh CA, Parnavelas JG (2007) Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 27(14):3875–3883CrossRefPubMedGoogle Scholar
  22. Gabay L, Lowell S, Rubin LL, Anderson DJ (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40(3):485–499CrossRefPubMedGoogle Scholar
  23. Gaillard A, Nasarre C, Roger M (2003) Early (E12) cortical progenitors can change their fate upon heterotopic transplantation. Eur J Neurosci 17(7):1375–1383CrossRefPubMedGoogle Scholar
  24. Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J, Espuny-Camacho I, Herpoel A, Passante L, Schiffmann SN, Gaillard A, Vanderhaeghen P (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455(7211):351–357CrossRefPubMedGoogle Scholar
  25. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439(7076):589–593CrossRefPubMedGoogle Scholar
  26. Graham ME, Ruma-Haynes P, Capes-Davis AG, Dunn JM, Tan TC, Valova VA, Robinson PJ, Jeffrey PL (2004) Multisite phosphorylation of doublecortin by cyclin-dependent kinase 5. Biochem J 381(Pt 2):471–481PubMedGoogle Scholar
  27. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Gotz M (2004) Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol Cell Neurosci 25(4):664–678CrossRefPubMedGoogle Scholar
  28. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391(2):85–100CrossRefPubMedGoogle Scholar
  29. Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229(1):15–30CrossRefPubMedGoogle Scholar
  30. Hatada I, Namihira M, Morita S, Kimura M, Horii T, Nakashima K (2008) Astrocyte-specific genes are generally demethylated in neural precursor cells prior to astrocytic differentiation. PLoS ONE 3(9):e3189CrossRefPubMedGoogle Scholar
  31. Heck N, Kilb W, Reiprich P, Kubota H, Furukawa T, Fukuda A, Luhmann HJ (2007) GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex 17(1):138–148CrossRefPubMedGoogle Scholar
  32. Hennou S, Khalilov I, Diabira D, Ben-Ari Y, Gozlan H (2002) Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci 16(2):197–208CrossRefPubMedGoogle Scholar
  33. Hutcheon B, Fritschy JM, Poulter MO (2004) Organization of GABA receptor alpha-subunit clustering in the developing rat neocortex and hippocampus. Eur J Neurosci 19(9):2475–2487CrossRefPubMedGoogle Scholar
  34. Jelitai M, Anderova M, Marko K, Kekesi K, Koncz P, Sykova E, Madarasz E (2004) Role of gamma-aminobutyric acid in early neuronal development: studies with an embryonic neuroectodermal stem cell clone. J Neurosci Res 76(6):801–811CrossRefPubMedGoogle Scholar
  35. Jelitai M, Anderova M, Chvatal A, Madarasz E (2007) Electrophysiological characterization of neural stem/progenitor cells during in vitro differentiation: study with an immortalized neuroectodermal cell line. J Neurosci Res 85(8):1606–1617CrossRefPubMedGoogle Scholar
  36. Johnson MA, Weick JP, Pearce RA, Zhang SC (2007) Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci 27(12):3069–3077CrossRefPubMedGoogle Scholar
  37. Kallur T, Darsalia V, Lindvall O, Kokaia Z (2006) Human fetal cortical and striatal neural stem cells generate region-specific neurons in vitro and differentiate extensively to neurons after intrastriatal transplantation in neonatal rats. J Neurosci Res 84(8):1630–1644CrossRefPubMedGoogle Scholar
  38. Kang J, Huguenard JR, Prince DA (2000) Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons. J Neurophysiol 83(1):70–80PubMedGoogle Scholar
  39. Kim HT, Kim IS, Lee IS, Lee JP, Snyder EY, Park KI (2006) Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed. Exp Neurol 199(1):222–235CrossRefPubMedGoogle Scholar
  40. Klein C, Butt SJ, Machold RP, Johnson JE, Fishell G (2005) Cerebellum- and forebrain-derived stem cells possess intrinsic regional character. Development 132(20):4497–4508CrossRefPubMedGoogle Scholar
  41. Korngreen A, Sakmann B (2000) Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol 525(Pt 3):621–639CrossRefPubMedGoogle Scholar
  42. Lepore AC, Neuhuber B, Connors TM, Han SS, Liu Y, Daniels MP, Rao MS, Fischer I (2006) Long-term fate of neural precursor cells following transplantation into developing and adult CNS. Neuroscience 139(2):513–530CrossRefPubMedGoogle Scholar
  43. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A (2006) GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54(5):394–410CrossRefPubMedGoogle Scholar
  44. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15(6):1287–1298CrossRefPubMedGoogle Scholar
  45. Machon O, van den Bout CJ, Backman M, Rosok O, Caubit X, Fromm SH, Geronimo B, Krauss S (2002) Forebrain-specific promoter/enhancer D6 derived from the mouse Dach1 gene controls expression in neural stem cells. Neuroscience 112(4):951–966CrossRefPubMedGoogle Scholar
  46. Machon O, Backman M, Krauss S, Kozmik Z (2005) The cellular fate of cortical progenitors is not maintained in neurosphere cultures. Mol Cell Neurosci 30(3):388–397CrossRefPubMedGoogle Scholar
  47. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127(24):5253–5263PubMedGoogle Scholar
  48. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Gotz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37(5):751–764CrossRefPubMedGoogle Scholar
  49. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18(20):8111–8125PubMedGoogle Scholar
  50. McMahon SS, McDermott KW (2007) Developmental potential of radial glia investigated by transplantation into the developing rat ventricular system in utero. Exp Neurol 203(1):128–136CrossRefPubMedGoogle Scholar
  51. Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14(9):5399–5416PubMedGoogle Scholar
  52. Mitterdorfer J, Bean BP (2002) Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 22(23):10106–10115PubMedGoogle Scholar
  53. Mo Z, Moore AR, Filipovic R, Ogawa Y, Kazuhiro I, Antic SD, Zecevic N (2007) Human cortical neurons originate from radial glia and neuron-restricted progenitors. J Neurosci 27(15):4132–4145CrossRefPubMedGoogle Scholar
  54. Modo M, Rezaie P, Heuschling P, Patel S, Male DK, Hodges H (2002) Transplantation of neural stem cells in a rat model of stroke: assessment of short-term graft survival and acute host immunological response. Brain Res 958(1):70–82CrossRefPubMedGoogle Scholar
  55. Mothe AJ, Kulbatski I, Parr A, Mohareb M, Tator CH (2008) Adult spinal cord stem/progenitor cells transplanted as neurospheres preferentially differentiate into oligodendrocytes in the adult rat spinal cord. Cell Transplant 17(7):735–751CrossRefPubMedGoogle Scholar
  56. Neprasova H, Anderova M, Petrik D, Vargova L, Kubinova S, Chvatal A, Sykova E (2007) High extracellular K(+) evokes changes in voltage-dependent K(+) and Na (+) currents and volume regulation in astrocytes. Pflugers Arch 453(6):839–849CrossRefPubMedGoogle Scholar
  57. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714–720CrossRefPubMedGoogle Scholar
  58. Ono K, Takebayashi H, Ikeda K, Furusho M, Nishizawa T, Watanabe K, Ikenaka K (2008) Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. Dev Biol 320(2):456–468CrossRefPubMedGoogle Scholar
  59. Owens DF, Liu X, Kriegstein AR (1999) Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J Neurophysiol 82(2):570–583PubMedGoogle Scholar
  60. Pagani F, Lauro C, Fucile S, Catalano M, Limatola C, Eusebi F, Grassi F (2006) Functional properties of neurons derived from fetal mouse neurospheres are compatible with those of neuronal precursors in vivo. J Neurosci Res 83(8):1494–1501CrossRefPubMedGoogle Scholar
  61. Parmar M, Skogh C, Englund U (2003) A transplantation study of expanded human embryonic forebrain precursors: evidence for selection of a specific progenitor population. Mol Cell Neurosci 23(4):531–543CrossRefPubMedGoogle Scholar
  62. Parnavelas JG, Alifragis P, Nadarajah B (2002) The origin and migration of cortical neurons. Prog Brain Res 136:73–80CrossRefPubMedGoogle Scholar
  63. Parr AM, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, Tator CH (2008) Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155(3):760–770CrossRefPubMedGoogle Scholar
  64. Parras CM, Hunt C, Sugimori M, Nakafuku M, Rowitch D, Guillemot F (2007) The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci 27(16):4233–4242CrossRefPubMedGoogle Scholar
  65. Piao JH, Odeberg J, Samuelsson EB, Kjaeldgaard A, Falci S, Seiger A, Sundstrom E, Akesson E (2006) Cellular composition of long-term human spinal cord- and forebrain-derived neurosphere cultures. J Neurosci Res 84(3):471–482CrossRefPubMedGoogle Scholar
  66. Picken Bahrey HL, Moody WJ (2003) Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol 89(4):1761–1773CrossRefPubMedGoogle Scholar
  67. Piper DR, Mujtaba T, Rao MS, Lucero MT (2000) Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J Neurophysiol 84(1):534–548PubMedGoogle Scholar
  68. Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28(1):69–80CrossRefPubMedGoogle Scholar
  69. Roelofs RF, Fischer DF, Houtman SH, Sluijs JA, Van Haren W, Van Leeuwen FW, Hol EM (2005) Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 52(4):289–300CrossRefPubMedGoogle Scholar
  70. Shmueli A, Gdalyahu A, Sapoznik S, Sapir T, Tsukada M, Reiner O (2006) Site-specific dephosphorylation of doublecortin (DCX) by protein phosphatase 1 (PP1). Mol Cell Neurosci 32(1–2):15–26CrossRefPubMedGoogle Scholar
  71. Smith DO, Rosenheimer JL, Kalil RE (2008) Delayed rectifier and A-type potassium channels associated with Kv 2.1 and Kv 4.3 expression in embryonic rat neural progenitor cells. PLoS ONE 3(2):e1604CrossRefPubMedGoogle Scholar
  72. Sun W, Buzanska L, Domanska-Janik K, Salvi RJ, Stachowiak MK (2005) Voltage-sensitive and ligand-gated channels in differentiating neural stem-like cells derived from the nonhematopoietic fraction of human umbilical cord blood. Stem Cells 23(7):931–945CrossRefPubMedGoogle Scholar
  73. Sun J, Gao Q, Miller K, Wang X, Wang J, Liu W, Bao L, Zhang J, Zhang L, Poon WS, Gao Y (2007) Dopaminergic differentiation of grafted GFP transgenic neuroepithelial stem cells in the brain of a rat model of Parkinson’s disease. Neurosci Lett 420(1):23–28CrossRefPubMedGoogle Scholar
  74. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17(1):58–69PubMedGoogle Scholar
  75. Tamamaki N, Nakamura K, Okamoto K, Kaneko T (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41(1):51–60CrossRefPubMedGoogle Scholar
  76. Tanaka T, Serneo FF, Tseng HC, Kulkarni AB, Tsai LH, Gleeson JG (2004) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41(2):215–227CrossRefPubMedGoogle Scholar
  77. Tateishi N, Shimoda T, Manako J, Katsumata S, Shinagawa R, Ohno H (2006) Relevance of astrocytic activation to reductions of astrocytic GABAA receptors. Brain Res 1089(1):79–91CrossRefPubMedGoogle Scholar
  78. Vorasubin B, Weedin J, Saljooque F, Wilkes N, Eng M, HS U (2007) Selective differentiation of central nervous system-derived stem cells in response to cues from specific regions of the developing brain. J Neurosurg 107(1):145–154CrossRefPubMedGoogle Scholar
  79. Vreugdenhil E, Kolk SM, Boekhoorn K, Fitzsimons CP, Schaaf M, Schouten T, Sarabdjitsingh A, Sibug R, Lucassen PJ (2007) Doublecortin-like, a microtubule-associated protein expressed in radial glia, is crucial for neuronal precursor division and radial process stability. Eur J Neurosci 25(3):635–648CrossRefPubMedGoogle Scholar
  80. Wang DD, Kriegstein AR (2008) GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci 28(21):5547–5558CrossRefPubMedGoogle Scholar
  81. Wang W, Jin K, Mao XO, Close N, Greenberg DA, Xiong ZG (2008) Electrophysiological properties of mouse cortical neuron progenitors differentiated in vitro and in vivo. Int J Clin Exp Med 1(2):145–153PubMedGoogle Scholar
  82. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD (1985) Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17(5):497–504CrossRefPubMedGoogle Scholar
  83. Webber DJ, Bradbury EJ, McMahon SB, Minger SL (2007) Transplanted neural progenitor cells survive and differentiate but achieve limited functional recovery in the lesioned adult rat spinal cord. Regen Med 2(6):929–945CrossRefPubMedGoogle Scholar
  84. Wei P, Liu J, Zhou HL, Han ZT, Wu QY, Pang JX, Liu S, Wang TH (2007) Effects of engrafted neural stem cells derived from GFP transgenic mice in Parkinson’s diseases rats. Neurosci Lett 419(1):49–54CrossRefPubMedGoogle Scholar
  85. Westerlund U, Moe MC, Varghese M, Berg-Johnsen J, Ohlsson M, Langmoen IA, Svensson M (2003) Stem cells from the adult human brain develop into functional neurons in culture. Exp Cell Res 289(2):378–383CrossRefPubMedGoogle Scholar
  86. Wu SX, Goebbels S, Nakamura K, Kometani K, Minato N, Kaneko T, Nave KA, Tamamaki N (2005) Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci USA 102(47):17172–17177CrossRefPubMedGoogle Scholar
  87. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A (2004) Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557(Pt 3):829–841CrossRefPubMedGoogle Scholar
  88. Yang H, Mujtaba T, Venkatraman G, Wu YY, Rao MS, Luskin MB (2000) Region-specific differentiation of neural tube-derived neuronal restricted progenitor cells after heterotopic transplantation. Proc Natl Acad Sci USA 97(24):13366–13371CrossRefPubMedGoogle Scholar
  89. Yasuda T, Bartlett PF, Adams DJ (2008) K(ir) and K(v) channels regulate electrical properties and proliferation of adult neural precursor cells. Mol Cell Neurosci 37(2):284–297CrossRefPubMedGoogle Scholar
  90. Zhou FM, Hablitz JJ (1996) Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16(3):1131–1139PubMedGoogle Scholar
  91. Zhou M, Schools GP, Kimelberg HK (2006) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95(1):134–143CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Iva Prajerova
    • 1
    • 2
  • Pavel Honsa
    • 1
    • 2
  • Alexandr Chvatal
    • 1
    • 2
    • 3
  • Miroslava Anderova
    • 1
    • 3
  1. 1.Laboratory of Neurobiology, Department of Cellular NeurophysiologyInstitute of Experimental Medicine ASCR v.v.i.Prague 4Czech Republic
  2. 2.Second Medical Faculty, Department of NeuroscienceCharles UniversityPrague 5Czech Republic
  3. 3.Second Medical Faculty, Center for Cell Therapy and Tissue RepairCharles UniversityPrague 5Czech Republic

Personalised recommendations