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Neural Plasticity
Volume 2011, Article ID 384216, 11 pages
http://dx.doi.org/10.1155/2011/384216
Review Article

GABAergic Neuronal Precursor Grafting: Implications in Brain Regeneration and Plasticity

1Department of Cell Therapy and Regenerative Medicine, Andalusian Center for Molecular Biology and Regenerative Medicine (CABIMER), 41092 Seville, Spain
2Stem Cell and Neurogenesis Unit, Division of Neuroscience, San Raffaele Scientific Institute, 20132 Milan, Italy

Received 23 February 2011; Accepted 11 April 2011

Academic Editor: Graziella Di Cristo

Copyright © 2011 Manuel Alvarez Dolado and Vania Broccoli. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. W. Olsen, “GABA,” in Neuropsychopharmacology: The Fifth Generation of Progress, K. L. Davis et al., Ed., pp. 159–168, American College of Neuropsychopharmacology, 2002. View at Google Scholar
  2. M. Watanabe, K. Maemura, K. Kanbara, T. Tamayama, and H. Hayasaki, “GABA and GABA receptors in the central nervous system and other organs,” International Review of Cytology, vol. 213, pp. 1–47, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Gajcy, S. Lochynski, and T. Librowski, “A role of GABA analogues in the treatment of neurological diseases,” Current Medicinal Chemistry, vol. 17, no. 22, pp. 2338–2347, 2010. View at Google Scholar
  4. A. Galvan and T. Wichmann, “GABAergic circuits in the basal ganglia and movement disorders,” Progress in Brain Research, vol. 160, pp. 287–312, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. S. R. Kleppner and A. J. Tobin, “GABA signalling: therapeutic targets for epilepsy, Parkinson's disease and Huntington's disease,” Expert Opinion on Therapeutic Targets, vol. 5, no. 2, pp. 219–239, 2001. View at Google Scholar
  6. Y. Ben-Ari, “Seizures beget seizures: the quest for GABA as a key player,” Critical Reviews in Neurobiology, vol. 18, no. 1-2, pp. 135–144, 2006. View at Google Scholar · View at Scopus
  7. K. G. Lloyd, L. Bossi, P. L. Morselli, C. Munari, M. Rougier, and H. Loiseau, “Alterations of GABA-mediated synaptic transmission in human epilepsy,” Advances in neurology, vol. 44, pp. 1033–1044, 1986. View at Google Scholar · View at Scopus
  8. D. M. Treiman, “GABAergic mechanisms in epilepsy,” Epilepsia, vol. 42, no. 3, pp. 8–12, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Lindvall and A. Björklund, “Intracerebral grafting of inhibitory neurons. A new strategy for seizure suppression in the central nervous system,” Advances in neurology, vol. 57, pp. 561–569, 1992. View at Google Scholar · View at Scopus
  10. O. Isacson, P. Brundin, and P. A. T. Kelly, “Functional neuronal replacement by grafted striatal neurones in the ibotenic acid-lesioned rat striatum,” Nature, vol. 311, no. 5985, pp. 458–460, 1984. View at Google Scholar · View at Scopus
  11. A. Björklund and O. Lindvall, “Cell replacement therapies for central nervous system disorders,” Nature Neuroscience, vol. 3, no. 6, pp. 537–544, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. J. G. Emsley, B. D. Mitchell, S. S. P. Magavi, P. Arlotta, and J. D. Macklis, “The repair of complex neuronal circuitry by transplanted and endogenous precursors,” NeuroRx, vol. 1, no. 4, pp. 452–471, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. W. Löscher, U. Ebert, H. Lehmann, C. Rosenthal, and G. Nikkhah, “Seizure suppression in kindling epilepsy by grafts of fetal GABAergic neurons in rat substantia nigra,” Journal of Neuroscience Research, vol. 51, no. 2, pp. 196–209, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Thompson, V. Anantharam, S. Behrstock, E. Bongarzone, A. Campagnoni, and A. J. Tobin, “Conditionally immortalized cell lines, engineered to produce and release GABA, modulate the development of behavioral seizures,” Experimental Neurology, vol. 161, no. 2, pp. 481–489, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. K. W. Thompson and L. M. Suchomelova, “Transplants of cells engineered to produce GABA suppress spontaneous seizures,” Epilepsia, vol. 45, no. 1, pp. 4–12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Amariglio, A. Hirshberg, and B. W. Scheithauer, “Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient,” PLoS Medicine, vol. 6, no. 2, Article ID e1000029, 2009. View at Publisher · View at Google Scholar · View at PubMed
  17. F. Erdö, C. Bührle, and J. Blunk, “Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke,” Journal of Cerebral Blood Flow and Metabolism, vol. 23, no. 7, pp. 780–785, 2003. View at Google Scholar · View at Scopus
  18. M. Alvarez-Dolado, M. E. Calcagnotto, and K. M. Karkar, “Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain,” Journal of Neuroscience, vol. 26, no. 28, pp. 7380–7389, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. O. Marín and J. L. R. Rubenstein, “A long, remarkable journey: tangential migration in the telencephalon,” Nature Reviews Neuroscience, vol. 2, no. 11, pp. 780–790, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. H. Wichterle, D. H. Turnbull, S. Nery, G. Fishell, and A. Alvarez-Buylla, “In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain,” Development, vol. 128, no. 19, pp. 3759–3771, 2001. View at Google Scholar · View at Scopus
  21. C. Wonders and S. A. Anderson, “Cortical interneurons and their origins,” Neuroscientist, vol. 11, no. 3, pp. 199–205, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. Q. Xu, I. Cobos, E. D. De La Cruz, J. L. Rubenstein, and S. A. Anderson, “Origins of cortical interneuron subtypes,” Journal of Neuroscience, vol. 24, no. 11, pp. 2612–2622, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. S. C. Baraban, D. G. Southwell, and R. C. Estrada, “Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 36, pp. 15472–15477, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. M. E. Calcagnotto, L. P. Ruiz, M. M. Blanco et al., “Effect of neuronal precursor cells derived from medial ganglionic eminence in an acute epileptic seizure model,” Epilepsia, vol. 51, supplement s3, pp. 71–75, 2010. View at Publisher · View at Google Scholar · View at PubMed
  25. M. E. Calcagnotto, I. Zipancic, M. Piquer-Gil, L. E. Mello, and M. Álvarez-Dolado, “Grafting of GABAergic precursors rescues deficits in hippocampal inhibition,” Epilepsia, vol. 51, supplement s3, pp. 66–70, 2010. View at Publisher · View at Google Scholar · View at PubMed
  26. V. Martínez-Cerdeño, S. C. Noctor, A. Espinosa et al., “Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats,” Cell Stem Cell, vol. 6, no. 3, pp. 238–250, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. B. Waldau, B. Hattiangady, R. Kuruba, and A. K. Shetty, “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, vol. 28, no. 7, pp. 1153–1164, 2010. View at Publisher · View at Google Scholar · View at PubMed
  28. I. Zipancic, M. E. Calcagnotto, M. Piquer-Gil, L. E. Mello, and M. Álvarez-Dolado, “Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility,” Cell Transplantation, vol. 19, no. 5, pp. 549–564, 2010. View at Publisher · View at Google Scholar · View at PubMed
  29. G. L. Holmes and Q. Zhao, “Choosing the correct antiepileptic drugs: from animal studies to the clinic,” Pediatric Neurology, vol. 38, no. 3, pp. 151–162, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. H. S. White, M. D. Smith, and K. S. Wilcox, “Mechanisms of action of antiepileptic drugs,” International Review of Neurobiology, vol. 81, pp. 85–110, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. P. Kwan and M. J. Brodie, “Early identification of refractory epilepsy,” New England Journal of Medicine, vol. 342, no. 5, pp. 314–319, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. W. Löscher, “Mechanisms of drug resistance in status epilepticus,” Epilepsia, vol. 48, no. 8, pp. 74–77, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. J. S. Duncan, “The outcome of epilepsy surgery,” Journal of Neurology Neurosurgery and Psychiatry, vol. 70, no. 4, p. 432, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. K. E. Nilsen and H. R. Cock, “Focal treatment for refractory epilepsy: hope for the future?” Brain Research Reviews, vol. 44, no. 2-3, pp. 141–153, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. A. R. Kriegstein and A. Pitkänen, “Commentary: the prospect of cell-based therapy for epilepsy,” Neurotherapeutics, vol. 6, no. 2, pp. 295–299, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. J. Y. Sebe and S. C. Baraban, “The promise of an interneuron-based cell therapy for epilepsy,” Developmental Neurobiology, vol. 71, no. 1, pp. 107–117, 2011. View at Publisher · View at Google Scholar
  37. K. Thompson, “Transplantation of GABA-producing cells for seizure control in models of temporal lobe epilepsy,” Neurotherapeutics, vol. 6, no. 2, pp. 284–294, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. C. G. Castillo, S. Mendoza, W. J. Freed, and M. Giordano, “Intranigral transplants of immortalized GABAergic cells decrease the expression of kainic acid-induced seizures in the rat,” Behavioural Brain Research, vol. 171, no. 1, pp. 109–115, 2006. View at Publisher · View at Google Scholar · View at PubMed
  39. C. G. Castillo, S. Mendoza-Trejo, M. B. Aguilar, W. J. Freed, and M. Giordano, “Intranigral transplants of a GABAergic cell line produce long-term alleviation of established motor seizures,” Behavioural Brain Research, vol. 193, no. 1, pp. 17–27, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. A. Fine, B. S. Meldrum, and S. Patel, “Modulation of experimentally induced epilepsy by intracerebral grafts of fetal GABAergic neurons,” Neuropsychologia, vol. 28, no. 6, pp. 627–634, 1990. View at Publisher · View at Google Scholar · View at Scopus
  41. J. R. Stevens, I. Phillips, W. J. Freed, and M. Poltorak, “Cerebral transplants for seizures: preliminary results,” Epilepsia, vol. 29, no. 6, pp. 731–737, 1988. View at Google Scholar · View at Scopus
  42. M. W. Nolte, W. Löscher, C. Herden, W. J. Freed, and M. Gernert, “Benefits and risks of intranigral transplantation of GABA-producing cells subsequent to the establishment of kindling-induced seizures,” Neurobiology of Disease, vol. 31, no. 3, pp. 342–354, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. P. Behrstock, V. Anantharam, K. W. Thompson, E. S. Schweitzer, and A. J. Tobin, “Conditionally-immortalized astrocytic cell line expresses GAD and secretes GABA under tetracycline regulation,” Journal of Neuroscience Research, vol. 60, no. 3, pp. 302–310, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Gernert, K. W. Thompson, W. Löscher, and A. J. Tobin, “Genetically engineered GABA-producing cells demonstrate anticonvulsant effects and long-term transgene expression when transplanted into the central piriform cortex of rats,” Experimental Neurology, vol. 176, no. 1, pp. 183–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. X. Maisano, J. Carpentino, S. Becker et al., “Embryonic stem cell-derived neural precursor grafts for treatment of temporal lobe epilepsy,” Neurotherapeutics, vol. 6, no. 2, pp. 263–277, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. A. K. Shetty and B. Hattiangady, “Concise review: prospects of stem cell therapy for temporal lobe epilepsy,” Stem Cells, vol. 25, no. 10, pp. 2396–2407, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. M. J. Evans and M. H. Kaufman, “Establishment in culture of pluripotential cells from mouse embryos,” Nature, vol. 292, no. 5819, pp. 154–156, 1981. View at Google Scholar · View at Scopus
  48. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar · View at Scopus
  49. S. Temple, “The development of neural stem cells,” Nature, vol. 414, no. 6859, pp. 112–117, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. A. Gritti, E. A. Parati, L. Cova et al., “Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor,” Journal of Neuroscience, vol. 16, no. 3, pp. 1091–1100, 1996. View at Google Scholar · View at Scopus
  51. A. L. Vescovi, B. A. Reynolds, D. D. Fraser, and S. Weiss, “bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells,” Neuron, vol. 11, no. 5, pp. 951–966, 1993. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Jain, R. J. E. Armstrong, P. Tyers, R. A. Barker, and A. E. Rosser, “GABAergic immunoreactivity is predominant in neurons derived from expanded human neural precursor cells in vitro,” Experimental Neurology, vol. 182, no. 1, pp. 113–123, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. J. J. Westmoreland, C. R. Hancock, and B. G. Condie, “Neuronal development of embryonic stem cells: a model of GABAergic neuron differentiation,” Biochemical and Biophysical Research Communications, vol. 284, no. 3, pp. 674–680, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. C. Rüschenschmidt, P. G. Koch, O. Brüstle, and H. Beck, “Functional properties of ES cell-derived neurons engrafted into the hippocampus of adult normal and chronically epileptic rats,” Epilepsia, vol. 46, no. 5, pp. 174–183, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. J. E. Carpentino, N. W. Hartman, L. B. Grabel, and J. R. Naegele, “Region-specific differentiation of embryonic stem cell-derived neural progenitor transplants into the adult mouse hippocampus following seizures,” Journal of Neuroscience Research, vol. 86, no. 3, pp. 512–524, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. A. Shindo, T. Nakamura, Y. Matsumoto et al., “Seizure suppression in amygdala-kindled mice by transplantation of neural stem/progenitor cells derived from mouse embryonic stem cells,” Neurologia Medico-Chirurgica, vol. 50, no. 2, pp. 98–105, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Chatzi, R. H. Scott, J. Pu et al., “Derivation of homogeneous GABAergic neurons from mouse embryonic stem cells,” Experimental Neurology, vol. 217, no. 2, pp. 407–416, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. A. M. Maroof, K. Brown, S. H. Shi, L. Studer, and S. A. Anderson, “Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells,” Journal of Neuroscience, vol. 30, no. 13, pp. 4667–4675, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. A. K. Shetty and B. Hattiangady, “Restoration of calbindin after fetal hippocampal CA3 cell grafting into the injured hippocampus in a rat model of temporal lobe epilepsy,” Hippocampus, vol. 17, no. 10, pp. 943–956, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. A. K. Shetty and D. A. Turner, “Development of fetal hippocampal grafts in intact and lesioned hippocampus,” Progress in Neurobiology, vol. 50, no. 5-6, pp. 597–653, 1996. View at Publisher · View at Google Scholar · View at Scopus
  61. A. K. Shetty and D. A. Turner, “Development of long-distance efferent projections from fetal hippocampal grafts depends upon pathway specificity and graft location in kainate-lesioned adult hippocampus,” Neuroscience, vol. 76, no. 4, pp. 1205–1219, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. A. K. Shetty and D. A. Turner, “Fetal hippocampal cells grafted to kainate-lesioned CA3 region of adult hippocampus suppress aberrant supragranular sprouting of host mossy fibers,” Experimental Neurology, vol. 143, no. 2, pp. 231–245, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. A. K. Shetty and D. A. Turner, “Fetal hippocampal grafts containing CA3 cells restore host hippocampal glutamate decarboxylase-positive interneuron numbers in a rat model of temporal lobe epilepsy,” Journal of Neuroscience, vol. 20, no. 23, pp. 8788–8801, 2000. View at Google Scholar · View at Scopus
  64. A. K. Shetty, V. Zaman, and B. Hattiangady, “Repair of the injured adult hippocampus through graft-mediated modulation of the plasticity of the dentate gyrus in a rat model of temporal lobe epilepsy,” Journal of Neuroscience, vol. 25, no. 37, pp. 8391–8401, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. A. K. Shetty, V. Zaman, and D. A. Turner, “Pattern of long-distance projections from fetal hippocampal field CA3 and CA1 cell grafts in lesioned CA3 of adult hippocampus follows intrinsic character of respective donor cells,” Neuroscience, vol. 99, no. 2, pp. 243–255, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. B. Hattiangady, M. S. Rao, and A. K. Shetty, “Grafting of striatal precursor cells into hippocampus shortly after status epilepticus restrains chronic temporal lobe epilepsy,” Experimental Neurology, vol. 212, no. 2, pp. 468–481, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. K. Chu, M. Kim, K. H. Jung et al., “Human neural stem cell transplantation reduces spontaneous recurrent seizures following pilocarpine-induced status epilepticus in adult rats,” Brain Research, vol. 1023, no. 2, pp. 213–221, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. J. L. Martin and R. S. Sloviter, “Focal inhibitory interneuron loss and principal cell hyperexcitability in the rat hippocampus after microinjection of a neurotoxic conjugate of saporin and a peptidase-resistant analog of substance P,” Journal of Comparative Neurology, vol. 436, no. 2, pp. 127–152, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. M. E. Calcagnotto, M. F. Paredes, T. Tihan, N. M. Barbaro, and S. C. Baraban, “Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia,” Journal of Neuroscience, vol. 25, no. 42, pp. 9649–9657, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. I. Cobos, M. E. Calcagnotto, A. J. Vilaythong et al., “Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy,” Nature Neuroscience, vol. 8, no. 8, pp. 1059–1068, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  71. H. S. White, “Preclinical development of antiepileptic drugs: past, present, and future directions,” Epilepsia, vol. 44, no. 7, pp. 2–8, 2003. View at Google Scholar · View at Scopus
  72. I. Kanter-Schlifke, L. Fjord-Larsen, P. Kusk, M. Ängehagen, L. Wahlberg, and M. Kokaia, “GDNF released from encapsulated cells suppresses seizure activity in the epileptic hippocampus,” Experimental Neurology, vol. 216, no. 2, pp. 413–419, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles, “On the origin of interictal activity in human temporal lobe epilepsy in vitro,” Science, vol. 298, no. 5597, pp. 1418–1421, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. L. Uva, M. Avoli, and M. De Curtis, “Synchronous GABA-receptor-dependent potentials in limbic areas of the in-vitro isolated adult guinea pig brain,” European Journal of Neuroscience, vol. 29, no. 5, pp. 911–920, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. G. Panuccio, G. Curia, A. Colosimo, G. Cruccu, and M. Avoli, “Epileptiform synchronization in the cingulate cortex,” Epilepsia, vol. 50, no. 3, pp. 521–536, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. J. Luo, M. G. Kaplitt, H. L. Fitzsimons et al., “Subthalamic GAD gene therapy in a Parkinson's disease rat model,” Science, vol. 298, no. 5592, pp. 425–429, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. M. G. Kaplitt, A. Feigin, C. Tang et al., “Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial,” Lancet, vol. 369, no. 9579, pp. 2097–2105, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. O. Lindvall, P. Brundin, H. Widner et al., “Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease,” Science, vol. 247, no. 4942, pp. 574–577, 1990. View at Google Scholar · View at Scopus
  79. S. B. Dunnett, A. Björklund, and O. Lindvall, “Cell therapy in Parkinson's disease—stop or go?” Nature Reviews Neuroscience, vol. 2, no. 5, pp. 365–369, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. C. Winkler, D. Kirik, and A. Björklund, “Cell transplantation in Parkinson's disease: how can we make it work?” Trends in Neurosciences, vol. 28, no. 2, pp. 86–92, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. P. Brundin, R. A. Barker, and M. Parmar, “Neural grafting in Parkinson's disease. Problems and possibilities,” Progress in Brain Research, vol. 184, pp. 265–294, 2010. View at Publisher · View at Google Scholar
  82. M. Politis, K. Wu, and C. Loane, “Serotonergic neurons mediate dyskinesia side effects in Parkinson's patients with neural transplants,” Science Translational Medicine, vol. 2, no. 38, pp. 38–46, 2010. View at Publisher · View at Google Scholar · View at PubMed
  83. E. Hedlund and T. Perlmann, “Neuronal cell replacement in parkinson's disease,” Journal of Internal Medicine, vol. 266, no. 4, pp. 358–371, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. V. Martínez-Cerdeño, S. C. Noctor, A. Espinosa et al., “Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats,” Cell Stem Cell, vol. 6, no. 3, pp. 238–250, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. T. Karayannis and G. Fishell, “Inhibition as a transplant-mediated therapy: a new paradigm for treating Parkinson's?” Cell Stem Cell, vol. 6, no. 3, pp. 184–185, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. M. M. Daadi, H. L. Sang, A. Arac et al., “Functional engraftment of the medial ganglionic eminence cells in experimental stroke model,” Cell Transplantation, vol. 18, no. 7, pp. 815–826, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. T. K. Hensch, “Critical period plasticity in local cortical circuits,” Nature Reviews Neuroscience, vol. 6, no. 11, pp. 877–888, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. N. Berardi, T. Pizzorusso, and L. Maffei, “Critical periods during sensory development,” Current Opinion in Neurobiology, vol. 10, no. 1, pp. 138–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  89. H. Morishita and T. K. Hensch, “Critical period revisited: impact on vision,” Current Opinion in Neurobiology, vol. 18, no. 1, pp. 101–107, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. T. K. Hensch, “Critical period regulation,” Annual Review of Neuroscience, vol. 27, pp. 549–579, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. H. Katagiri, M. Fagiolini, and T. K. Hensch, “Optimization of somatic inhibition at critical period onset in mouse visual cortex,” Neuron, vol. 53, no. 6, pp. 805–812, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. M. Fagiolini, J. M. Fritschy, K. Löw, H. Möhler, U. Rudolph, and T. K. Hensch, “Specific GABAA circuits for visual cortical plasticity,” Science, vol. 303, no. 5664, pp. 1681–1683, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  93. G. Di Cristo, B. Chattopadhyaya, S. J. Kuhlman et al., “Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity,” Nature Neuroscience, vol. 10, no. 12, pp. 1569–1577, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. D. G. Southwell, R. C. Froemke, A. Alvarez-Buylla, M. P. Stryker, and S. P. Gandhi, “Cortical plasticity induced by inhibitory neuron transplantation,” Science, vol. 327, no. 5969, pp. 1145–1148, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. M. Fagiolini and T. K. Hensch, “Inhibitory threshold for critical-period activation in primary visual cortex,” Nature, vol. 404, no. 6774, pp. 183–186, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  96. S. P. Gandhi, Y. Yanagawa, and M. P. Stryker, “Delayed plasticity of inhibitory neurons in developing visual cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 43, pp. 16797–16802, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  97. A. Gritti, P. Frölichsthal-Schoeller, R. Galli et al., “Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain,” Journal of Neuroscience, vol. 19, no. 9, pp. 3287–3297, 1999. View at Google Scholar · View at Scopus
  98. L. Conti, S. M. Pollard, T. Gorba et al., “Niche-independent symmetrical self-renewal of a mammalian tissue stem cell,” PLoS Biology, vol. 3, no. 9, article e283, 2005. View at Google Scholar
  99. C. Gregg and S. Weiss, “Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells,” Journal of Neuroscience, vol. 23, no. 37, pp. 11587–11601, 2003. View at Google Scholar · View at Scopus
  100. L. Conti and E. Cattaneo, “Neural stem cell systems: physiological players or in vitro entities?” Nature Reviews Neuroscience, vol. 11, no. 3, pp. 176–187, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. E. Colombo, S. G. Giannelli, and R. Galli, “Embryonic stem-derived versus somatic neural stem cells: a comparative analysis of their developmental potential and molecular phenotype,” Stem Cells, vol. 24, no. 4, pp. 825–834, 2006. View at Publisher · View at Google Scholar · View at PubMed
  102. M. Onorati, M. Binetti, L. Conti et al., “Preservation of positional identity in fetus-derived neural stem (NS) cells from different mouse central nervous system compartments,” Cellular and Molecular Life Sciences, vol. 68, no. 10, pp. 1769–1783, 2011. View at Publisher · View at Google Scholar · View at PubMed
  103. J. M. Baizabal, C. Valencia, G. Guerrero-Flores, and L. Covarrubias, “Telencephalic neural precursor cells show transient competence to interpret the dopaminergic niche of the embryonic midbrain,” Developmental Biology, vol. 349, no. 2, pp. 192–203, 2011. View at Publisher · View at Google Scholar · View at PubMed
  104. O. Machon, M. Backman, S. Krauss, and Z. Kozmik, “The cellular fate of cortical progenitors is not maintained in neurosphere cultures,” Molecular and Cellular Neuroscience, vol. 30, no. 3, pp. 388–397, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  105. T. Danjo, M. Eiraku, K. Muguruma et al., “Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed and combinatory treatment with extrinsic signals,” Journal of Neuroscience, vol. 31, no. 5, pp. 1919–1933, 2011. View at Publisher · View at Google Scholar · View at PubMed
  106. A. M. Maroof, K. Brown, S. H. Shi, L. Studer, and S. A. Anderson, “Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells,” Journal of Neuroscience, vol. 30, no. 13, pp. 4667–4675, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus