Table of Contents
ISRN Neuroscience
Volume 2013 (2013), Article ID 354136, 14 pages
http://dx.doi.org/10.1155/2013/354136
Review Article

The (Real) Neurogenic/Gliogenic Potential of the Postnatal and Adult Brain Parenchyma

Neuroscience Institute Cavalieri Ottolenghi (NICO), University of Turin, Regione Gonzole 10, 10043 Turin, Italy

Received 18 December 2012; Accepted 8 January 2013

Academic Editors: A. K. Clark, A. Grant, and B.-Y. Zeng

Copyright © 2013 Luca Bonfanti. 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. B. A. Reynolds and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992. View at Google Scholar · View at Scopus
  2. C. G. Gross, “Neurogenesis in the adult brain: death of a dogma,” Nature Reviews, vol. 1, no. 1, pp. 67–73, 2000. View at Google Scholar · View at Scopus
  3. F. H. Gage, “Mammalian neural stem cells,” Science, vol. 287, no. 5457, pp. 1433–1438, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Lois and A. Alvarez-Buylla, “Long-distance neuronal migration in the adult mammalian brain,” Science, vol. 264, no. 5162, pp. 1145–1148, 1994. View at Google Scholar · View at Scopus
  5. F. H. Gage, G. Kempermann, T. D. Palmer, D. A. Peterson, and J. Ray, “Multipotent progenitor cells in the adult dentate gyrus,” Journal of Neurobiology, vol. 36, pp. 249–266, 1998. View at Google Scholar
  6. E. Arenas, “Towards stem cell replacement therapies for Parkinson's disease,” Biochemical and Biophysical Research Communications, vol. 396, no. 1, pp. 152–156, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. O. Lindvall and Z. Kokaia, “Stem cells in human neurodegenerative disorders—time for clinical translation?” The Journal of Clinical Investigation, vol. 120, no. 1, pp. 29–40, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Bonfanti and G. Ponti, “Adult mammalian neurogenesis and the New Zealand white rabbit,” Veterinary Journal, vol. 175, no. 3, pp. 310–331, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Kriegstein and A. Alvarez-Buylla, “The glial nature of embryonic and adult neural stem cells,” Annual Review of Neuroscience, vol. 32, pp. 149–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Zhao, E. M. Teng, R. G. Summers Jr., G. L. Ming, and F. H. Gage, “Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus,” Journal of Neuroscience, vol. 26, no. 1, pp. 3–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Bonfanti, “From hydra regeneration to human brain structural plasticity: a long trip through narrowing roads,” The Scientific World Journal, vol. 11, pp. 1270–1299, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. P. J. Horner, A. E. Power, G. Kempermann et al., “Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord,” Journal of Neuroscience, vol. 20, no. 6, pp. 2218–2228, 2000. View at Google Scholar · View at Scopus
  13. M. R. L. Dawson, A. Polito, J. M. Levine, and R. Reynolds, “NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS,” Molecular and Cellular Neuroscience, vol. 24, no. 2, pp. 476–488, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. A. M. Butt, N. Hamilton, P. Hubbard, M. Pugh, and M. Ibrahim, “Synantocytes: the fifth element,” Journal of Anatomy, vol. 207, no. 6, pp. 695–706, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Nishiyama, M. Komitova, R. Suzuki, and X. Zhu, “Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity,” Nature Reviews Neuroscience, vol. 10, no. 1, pp. 9–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Trotter, K. Karram, and A. Nishiyama, “NG2 cells: properties, progeny and origin,” Brain Research Reviews, vol. 63, no. 1-2, pp. 72–82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. A. G. Dayer, K. M. Cleaver, T. Abouantoun, and H. A. Cameron, “New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors,” Journal of Cell Biology, vol. 168, no. 3, pp. 415–427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Luzzati, S. De Marchis, A. Fasolo, and P. Peretto, “Neurogenesis in the caudate nucleus of the adult rabbit,” Journal of Neuroscience, vol. 26, no. 2, pp. 609–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Ponti, P. Peretto, and L. Bonfanti, “Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits,” PLoS ONE, vol. 3, no. 6, Article ID e2366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. T. D. Palmer, E. A. Markakis, A. R. Willhoite, F. Safar, and F. H. Gage, “Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS,” Journal of Neuroscience, vol. 19, no. 19, pp. 8487–8497, 1999. View at Google Scholar · View at Scopus
  21. S. Belachew, R. Chittajallu, A. A. Aguirre et al., “Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons,” Journal of Cell Biology, vol. 161, no. 1, pp. 169–186, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Gould, A. J. Reeves, M. S. A. Graziano, and C. G. Gross, “Neurogenesis in the neocortex of adult primates,” Science, vol. 286, no. 5439, pp. 548–552, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. S. S. Magavi, B. R. Leavitt, and J. D. Macklis, “Induction of neurogenesis in the neocertex of adult mice,” Nature, vol. 405, no. 6789, pp. 951–955, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. D. R. Kornack and P. Rakic, “Cell proliferation without neurogenesis in adult primate neocortex,” Science, vol. 294, no. 5549, pp. 2127–2130, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall, “Neuronal replacement from endogenous precursors in the adult brain after stroke,” Nature Medicine, vol. 8, no. 9, pp. 963–970, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Nakatomi, T. Kuriu, S. Okabe et al., “Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors,” Cell, vol. 110, no. 4, pp. 429–441, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Thored, A. Arvidsson, E. Cacci et al., “Persistent production of neurons from adult brain stem cells during recovery after stroke,” Stem Cells, vol. 24, no. 3, pp. 739–747, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Luzzati, S. De Marchis, R. Parlato et al., “New striatal neurons in a mouse model of progressive striatal degeneration are generated in both the subventricular zone and the striatal parenchyma,” PLoS One, vol. 6, Article ID e25088, 2011. View at Google Scholar
  29. B. W. Lindsey and V. Tropepe, “A comparative framework for understanding the biological principles of adult neurogenesis,” Progress in Neurobiology, vol. 80, no. 6, pp. 281–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Clancy, R. B. Darlington, and B. L. Finlay, “Translating developmental time across mammalian species,” Neuroscience, vol. 105, no. 1, pp. 7–17, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Gritti and L. Bonfanti, “Neuronal-glial interactions in central nervous system neurogenesis: the neural stem cell perspective,” Neuron Glia Biology, vol. 3, no. 4, pp. 309–323, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Bonfanti and P. Peretto, “Adult neurogenesis in mammals—a theme with many variations,” European Journal of Neuroscience, vol. 34, pp. 930–950, 2011. View at Google Scholar
  33. G. H. Kuhn and K. Blomgren, “Developmental dysregulation of adult neurogenesis,” European Journal of Neuroscience, vol. 33, pp. 1115–1122, 2011. View at Google Scholar
  34. D. M. Feliciano and A. Bordey, “Newborn cortical neurons: only for neonates?” Trends in Neurosciences, vol. 36, no. 1, pp. 51–61, 2012. View at Google Scholar
  35. G. Ponti, P. Peretto, and L. Bonfanti, “A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum,” Developmental Biology, vol. 294, no. 1, pp. 168–180, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. W. D. Richardson, K. M. Young, R. B. Tripathi, and I. McKenzie, “NG2-glia as multipotent neural stem cells: fact or fantasy?” Neuron, vol. 70, no. 4, pp. 661–673, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Buffo, I. Rite, P. Tripathi et al., “Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 9, pp. 3581–3586, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. M. C. Raff, R. H. Miller, and M. Noble, “A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium,” Nature, vol. 303, no. 5916, pp. 390–396, 1983. View at Google Scholar · View at Scopus
  39. I. V. Yannas, Tissue and Organ Regeneration in Adults, Springer, New York, NY, USA, 2001.
  40. Y. Kozorovitskiy and E. Gould, “Adult neurogenesis: a mechanism for brain repair?” Journal of Clinical and Experimental Neuropsychology, vol. 25, no. 5, pp. 721–732, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Ferretti, “Is there a relationship between adult neurogenesis and neuron generation following injury across evolution?” European Journal of Neuroscience, vol. 34, pp. 951–962, 2011. View at Google Scholar
  42. L. Bonfanti, F. Rossi, and G. K. Zupanc, “Towards a comparative understanding of adult neurogenesis,” European Journal of Neuroscience, vol. 34, pp. 845–846, 2011. View at Google Scholar
  43. G. Martino, S. Pluchino, L. Bonfanti, and M. Schwartz, “Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells,” Physiological Reviews, vol. 91, pp. 1281–1304, 2011. View at Google Scholar
  44. G. K. H. Zupanc, “Neurogenesis and neuronal regeneration in the adult fish brain,” Journal of Comparative Physiology A, vol. 192, no. 6, pp. 649–670, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Grandel and M. Brand, “Comparative aspects of adult neural stem cell activity in vertebrates,” Development Genes and Evolution, vol. 223, pp. 131–147, 2013. View at Google Scholar
  46. U. S. Sohur, J. G. Emsley, B. D. Mitchell, and J. D. Macklis, “Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1473, pp. 1477–1497, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Ponti, P. Crociara, M. Armentano, and L. Bonfanti, “Adult neurogenesis without germinal layers: the “atypical” cerebellum of rabbits,” Archives Italiennes de Biologie, vol. 148, no. 2, pp. 147–158, 2010. View at Google Scholar · View at Scopus
  48. O. Koizumi and H. R. Bode, “Plasticity in the nervous system of adult hydra. III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location,” Journal of Neuroscience, vol. 11, no. 7, pp. 2011–2020, 1991. View at Google Scholar · View at Scopus
  49. Y. Umesono and K. Agata, “Evolution and regeneration of the planarian central nervous system,” Development Growth and Differentiation, vol. 51, no. 3, pp. 185–195, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. R. F. Sîrbulescu and G. K. H. Zupanc, “Spinal cord repair in regeneration-competent vertebrates: adult teleost fish as a model system,” Brain Research Reviews, vol. 67, no. 1-2, pp. 73–93, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Endo, J. Yoshino, K. Kado, and S. Tochinai, “Brain regeneration in anuran amphibians,” Development Growth and Differentiation, vol. 49, no. 2, pp. 121–129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. M. Lledo, M. Alonso, and M. S. Grubb, “Adult neurogenesis and functional plasticity in neuronal circuits,” Nature Reviews Neuroscience, vol. 7, no. 3, pp. 179–193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Kempermann, “New neurons for ‘survival of the fittest’,” Nature Reviews Neuroscience, vol. 13, pp. 727–736, 2012. View at Google Scholar
  54. K. Whalley, S. Gögel, S. Lange, and P. Ferretti, “Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord,” Developmental Biology, vol. 332, no. 2, pp. 234–245, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Jopling, E. Sleep, M. Raya, M. Martí, A. Raya, and J. C. I. Belmonte, “Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation,” Nature, vol. 464, no. 7288, pp. 606–609, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. A. L. Mescher and A. W. Neff, “Limb regeneration in amphibians: immunological considerations,” The Scientific World Journal, vol. 6, no. 1, pp. 1–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. Z. M. Weil, G. J. Norman, A. C. DeVries, and R. J. Nelson, “The injured nervous system: a Darwinian perspective,” Progress in Neurobiology, vol. 86, no. 1, pp. 48–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. K. M. Johnson, R. Boonstra, and J. M. Wojtowicz, “Hippocampal neurogenesis in food-storing red squirrels: the impact of age and spatial behavior,” Genes, Brain and Behavior, vol. 9, no. 6, pp. 583–591, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. J. M. Barker, R. Boonstra, and J. M. Wojtowicz, “From pattern to pourpose: how comparative studies contribute to understanding the function of adult neurogenesis,” European Journal of Neuroscience, vol. 34, pp. 963–977, 2011. View at Google Scholar
  60. N. Sanai, T. Nguyen, R. A. Ihrie et al., “Corridors of migrating neurons in the human brain and their decline during infancy,” Nature, vol. 478, pp. 382–386, 2011. View at Google Scholar
  61. M. V. Kokoeva, H. Yin, and J. S. Flier, “Neurogenesis in the hypothalamus of adult mice: potential role in energy balance,” Science, vol. 310, no. 5748, pp. 679–683, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. J. G. Emsley, B. D. Mitchell, G. Kempermann, and J. D. Macklis, “Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells,” Progress in Neurobiology, vol. 75, no. 5, pp. 321–341, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Ohira, T. Furuta, H. Hioki et al., “Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells,” Nature Neuroscience, vol. 13, no. 2, pp. 173–179, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. A. A. Pierce and A. W. Xu, “De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance,” Journal of Neuroscience, vol. 30, no. 2, pp. 723–730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. R. A. Ihrie and A. Álvarez-Buylla, “Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain,” Neuron, vol. 70, no. 4, pp. 674–686, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Peretto, C. Giachino, P. Aimar, A. Fasolo, and L. Bonfanti, “Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain,” Journal of Comparative Neurology, vol. 487, no. 4, pp. 407–427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Bonfanti and P. Peretto, “Radial glial origin of the adult neural stem cells in the subventricular zone,” Progress in Neurobiology, vol. 83, no. 1, pp. 24–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. W. Haubensak, A. Attardo, W. Denk, and W. B. Huttner, “Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3196–3201, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Voigt, “Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes,” Journal of Comparative Neurology, vol. 289, no. 1, pp. 74–88, 1989. View at Google Scholar · View at Scopus
  70. J. P. Mission, T. Takahashi, and V. S. Caviness, “Ontogeny of radial and other astroglial cells in murine cerebral cortex,” Glia, vol. 4, no. 2, pp. 138–148, 1991. View at Google Scholar · View at Scopus
  71. P. Malatesta, E. Hartfuss, and M. Götz, “Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neural lineage,” Development, vol. 127, no. 24, pp. 5253–5263, 2000. View at Google Scholar · View at Scopus
  72. S. C. Noctor, A. C. Flint, T. A. Weissman, R. S. Dammerman, and A. R. Kriegstein, “Neurons derived from radial glial cells establish radial units in neocortex,” Nature, vol. 409, no. 6821, pp. 714–720, 2001. View at Publisher · View at Google Scholar · View at Scopus
  73. F. T. Merkle, A. D. Tramontin, J. M. García-Verdugo, and A. Alvarez-Buylla, “Radial glia give rise to adult neural stem cells in the subventricular zone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 50, pp. 17528–17532, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. M. F. Eckenhoff and P. Rakic, “Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey,” Journal of Comparative Neurology, vol. 223, no. 1, pp. 1–21, 1984. View at Google Scholar · View at Scopus
  75. B. Seri, J. M. García-Verdugo, L. Collado-Morente, B. S. McEwen, and A. Alvarez-Buylla, “Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus,” Journal of Comparative Neurology, vol. 478, no. 4, pp. 359–378, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. E. D. Laywell, P. Rakic, V. G. Kukekov, E. C. Holland, and D. A. Steindler, “Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 25, pp. 13883–13888, 2000. View at Publisher · View at Google Scholar · View at Scopus
  77. M. V. Sofroniew, “Molecular dissection of reactive astrogliosis and glial scar formation,” Trends in Neurosciences, vol. 32, no. 12, pp. 638–647, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. T. M. Jessell, “Neuronal specification in the spinal cord: inductive signals and transcriptional codes,” Nature Reviews Genetics, vol. 1, no. 1, pp. 20–29, 2000. View at Google Scholar · View at Scopus
  79. H. Takebayashi, S. Yoshida, M. Sugimori et al., “Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3,” Mechanisms of Development, vol. 99, no. 1-2, pp. 143–148, 2000. View at Publisher · View at Google Scholar · View at Scopus
  80. N. P. Pringle and W. D. Richardson, “A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage,” Development, vol. 117, no. 2, pp. 525–533, 1993. View at Google Scholar · View at Scopus
  81. C. Poncet, C. Soula, F. Trousse et al., “Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: effects of notochord and floor plate grafts, and of sonic hedgehog,” Mechanisms of Development, vol. 60, no. 1, pp. 13–32, 1996. View at Publisher · View at Google Scholar · View at Scopus
  82. N. P. Pringle, W. P. Yu, S. Guthrie et al., “Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and Sonic hedgehog,” Developmental Biology, vol. 177, no. 1, pp. 30–42, 1996. View at Publisher · View at Google Scholar · View at Scopus
  83. B. C. Warf, J. Fok-Seang, and R. H. Miller, “Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord,” Journal of Neuroscience, vol. 11, no. 8, pp. 2477–2488, 1991. View at Google Scholar · View at Scopus
  84. A. Vallstedt, J. M. Klos, and J. Ericson, “Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain,” Neuron, vol. 45, no. 1, pp. 55–67, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. W. D. Richardson, N. Kessaris, and N. Pringle, “Oligodendrocyte wars,” Nature Reviews Neuroscience, vol. 7, no. 1, pp. 11–18, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. N. Tekki-Kessaris, R. Woodruff, A. C. Hall et al., “Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon,” Development, vol. 128, no. 13, pp. 2545–2554, 2001. View at Google Scholar · View at Scopus
  87. N. Kessaris, M. Fogarty, P. Iannarelli, M. Grist, M. Wegner, and W. D. Richardson, “Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage,” Nature Neuroscience, vol. 9, no. 2, pp. 173–179, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Nishiyama, X. H. Lin, N. Giese, C. H. Heldin, and W. B. Stallcup, “Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain,” Journal of Neuroscience Research, vol. 43, pp. 299–314, 1996. View at Google Scholar
  89. M. Diers-Fenger, F. Kirchhoff, H. Kettenmann, J. M. Levine, and J. Trotter, “AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia,” GLIA, vol. 34, no. 3, pp. 213–228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Berry, P. Hubbard, and A. M. Butt, “Cytology and lineage of NG2-positive glia,” Journal of Neurocytology, vol. 31, no. 6-7, pp. 457–467, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. J. M. Levine, F. Stincone, and Y. S. Lee, “Development and differentiation of glial precursor cells in the rat cerebellum.,” Glia, vol. 7, no. 4, pp. 307–321, 1993. View at Google Scholar · View at Scopus
  92. P. J. Bernier, A. Bédard, J. Vinet, M. Lévesque, and A. Parent, “Newly generated neurons in the amygdala and adjoining cortex of adult primates,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 17, pp. 11464–11469, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Gould, N. Vail, M. Wagers, and C. G. Gross, “Adult-generated hippocampal and neocortical neurons in macaques have a transient existence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10910–10917, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. J. S. Snyder, J. S. Choe, M. A. Clifford et al., “Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice,” Journal of Neuroscience, vol. 29, no. 46, pp. 14484–14495, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. G. Kempermann, E. J. Chesler, L. Lu, R. W. Williams, and F. H. Gage, “Natural variation and genetic covariance in adult hippocampal neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 3, pp. 780–785, 2006. View at Publisher · View at Google Scholar · View at Scopus
  96. P. J. Clark, R. A. Kohman, D. S. Miller, T. K. Bhattacharya, W. J. Brzezinska, and J. S. Rhodes, “Genetic influences on exercise-induced adult hippocampal neurogenesis across 12 divergent mouse strains,” Genes, Brain and Behavior, vol. 10, no. 3, pp. 345–353, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. I. Amrein, K. Isler, and H. P. Lipp, “Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage,” European Journal of Neuroscience, vol. 34, pp. 978–987, 2011. View at Google Scholar
  98. M. Zhao, S. Momma, K. Delfani et al., “Evidence for neurogenesis in the adult mammalian substantia nigra,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 13, pp. 7925–7930, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. L. E. Rivers, K. M. Young, M. Rizzi et al., “PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice,” Nature Neuroscience, vol. 11, no. 12, pp. 1392–1401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. F. Guo, Y. Maeda, J. Ma et al., “Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex,” Journal of Neuroscience, vol. 30, no. 36, pp. 12036–12049, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. S. H. Kang, M. Fukaya, J. K. Yang, J. D. Rothstein, and D. E. Bergles, “NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration,” Neuron, vol. 68, no. 4, pp. 668–681, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Frielingsdorf, K. Schwarz, P. Brundin, and P. Mohapel, “No evidence for new dopaminergic neurons in the adult mammalian substantia nigra,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 27, pp. 10177–10182, 2004. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Komitova, E. Perfilieva, B. Mattsson, P. S. Eriksson, and B. B. Johansson, “Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex,” Experimental Neurology, vol. 199, no. 1, pp. 113–121, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Vessal and C. Darian-Smith, “Adult neurogenesis occurs in primate sensorimotor cortex following cervical dorsal rhizotomy,” Journal of Neuroscience, vol. 30, no. 25, pp. 8613–8623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Mantamadiotis, T. Lemberger, S. C. Bleckmann et al., “Disruption of CREB function in brain leads to neurodegeneration,” Nature Genetics, vol. 31, no. 1, pp. 47–54, 2002. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Migaud, M. Batailler, S. Segura, A. Duittoz, I. Franceschini, and D. Pillon, “Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones,” European Journal of Neuroscience, vol. 32, no. 12, pp. 2042–2052, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. Y. Xu, N. Tamamaki, T. Noda et al., “Neurogenesis in the ependymal layer of the adult rat 3rd ventricle,” Experimental Neurology, vol. 192, no. 2, pp. 251–264, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. M. V. Kokoeva, H. Yin, and J. S. Flier, “Evidence for constitutive neural cell proliferation in the adult murine hypothalamus,” Journal of Comparative Neurology, vol. 505, no. 2, pp. 209–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. L. Bennett, M. Yang, G. Enikolopov, and L. Iacovitti, “Circumventricular organs: a novel site of neural stem cells in the adult brain,” Molecular and Cellular Neuroscience, vol. 41, no. 3, pp. 337–347, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Pérez-Martín, M. Cifuentes, J. M. Grondona et al., “IGF-I stimulates neurogenesis in the hypothalamus of adult rats,” European Journal of Neuroscience, vol. 31, pp. 1533–1548, 2010. View at Google Scholar
  111. K. Matsuzaki, M. Katakura, T. Hara, G. Li, M. Hashimoto, and O. Shido, “Proliferation of neuronal progenitor cells and neuronal differentiation in the hypothalamus are enhanced in heat-acclimated rats,” Pflugers Archiv European Journal of Physiology, vol. 458, no. 4, pp. 661–673, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Pekcec, W. Löscher, and H. Potschka, “Neurogenesis in the adult rat piriform cortex,” NeuroReport, vol. 17, no. 6, pp. 571–574, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. L. A. Shapiro, K. L. Ng, Q. Y. Zhou, and C. E. Ribak, “Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice,” NeuroReport, vol. 18, no. 10, pp. 981–985, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. M. A. Gómez-Climent, E. Castillo-Gómez, E. Varea et al., “A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood,” Cerebral Cortex, vol. 18, no. 10, pp. 2229–2240, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. T. Seki and Y. Arai, “Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat,” Anatomy and Embryology, vol. 184, no. 4, pp. 395–401, 1991. View at Google Scholar · View at Scopus
  116. L. Bonfanti, “PSA-NCAM in mammalian structural plasticity and neurogenesis,” Progress in Neurobiology, vol. 80, no. 3, pp. 129–164, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. L. Bonfanti and J. Nacher, “New scenarios for neuronal structural plasticity in non-neurogenic brain parenchyma: the case of cortical layer II immature neurons,” Progress in Neurobiology, vol. 98, pp. 1–15, 2012. View at Google Scholar
  118. E. Boda and A. Buffo, “Glial cells in non-germinal territories: insights into their stem/progenitor properties in the intact and injured nervous tissue,” Archives Italiennes de Biologie, vol. 148, no. 2, pp. 119–136, 2010. View at Google Scholar · View at Scopus
  119. W. B. Stallcup and L. Beasley, “Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan,” Journal of Neuroscience, vol. 7, no. 9, pp. 2737–2744, 1987. View at Google Scholar · View at Scopus
  120. R. Reynolds, M. Dawson, D. Papadopoulos et al., “The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS,” Journal of Neurocytology, vol. 31, no. 6-7, pp. 523–536, 2002. View at Publisher · View at Google Scholar · View at Scopus
  121. A. A. Aguirre, R. Chittajallu, S. Belachew, and V. Gallo, “NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus,” Journal of Cell Biology, vol. 165, no. 4, pp. 575–589, 2004. View at Publisher · View at Google Scholar · View at Scopus
  122. K. L. Ligon, S. P. J. Fancy, R. J. M. Franklin, and D. H. Rowitch, “Olig gene function in CNS development and disease,” GLIA, vol. 54, no. 1, pp. 1–10, 2006. View at Publisher · View at Google Scholar · View at Scopus
  123. R. Reynolds and R. Hardy, “Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo,” Journal of Neuroscience Research, vol. 47, pp. 455–470, 1997. View at Google Scholar
  124. Q. Zhou, S. Wang, and D. J. Anderson, “Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors,” Neuron, vol. 25, no. 2, pp. 331–343, 2000. View at Google Scholar · View at Scopus
  125. J. Bu, A. Banki, Q. Wu, and A. Nishiyama, “Increased NG2+ glial cell proliferation and oligodendrocyte generation in the hypomyelinating mutant shiverer,” GLIA, vol. 48, no. 1, pp. 51–63, 2004. View at Publisher · View at Google Scholar · View at Scopus
  126. R. J. Franklin and S. C. Barnett, “Do olfactory glia have advantages over Schwann cells for CNS repair?” Journal of Neuroscience Research, vol. 50, pp. 665–672, 1997. View at Google Scholar
  127. L. Dimou, C. Simon, F. Kirchhoff, H. Takebayashi, and M. Götz, “Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex,” Journal of Neuroscience, vol. 28, no. 41, pp. 10434–10442, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. A. Espinosa de los Monteros, R. Bernard, B. Tiller, P. Rouget, and J. de Vellis, “Grafting of fast blue labeled glial cells into neonatal rat brain: differential survival and migration among cell types,” International Journal of Developmental Neuroscience, vol. 11, no. 5, pp. 625–639, 1993. View at Publisher · View at Google Scholar · View at Scopus
  129. A. K. Groves, S. C. Barnett, R. J. M. Franklin et al., “Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells,” Nature, vol. 362, no. 6419, pp. 453–455, 1993. View at Publisher · View at Google Scholar · View at Scopus
  130. B. M. Riederer, “Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein,” Brain Research Bulletin, vol. 71, no. 6, pp. 541–558, 2007. View at Publisher · View at Google Scholar · View at Scopus
  131. C. Simon, M. Götz, and L. Dimou, “Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury,” GLIA, vol. 59, no. 6, pp. 869–881, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. X. Zhu, R. A. Hill, D. Dietrich, M. Komitova, R. Suzuki, and A. Nishiyama, “Age-dependent fate and lineage restriction of single NG2 cells,” Development, vol. 138, no. 4, pp. 745–753, 2011. View at Publisher · View at Google Scholar · View at Scopus
  133. S. Sugiarto, A. I. Persson, E. G. Munoz et al., “Asymmetric-defective oligodendrocyte progenitors are glioma precursors,” Cancer Cell, vol. 20, pp. 320–340, 2011. View at Google Scholar