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Injury-induced neurogenesis in the mammalian forebrain

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Abstract

It has been accepted that new neurons are added to the olfactory bulb and the hippocampal dentate gyrus throughout life in the healthy adult mammalian brain. Recent studies have clarified that brain insult raises the proliferation of neural stem cells/neural progenitor cells existing in the subventricular zone and the subgranular zone, which become sources of new neurons for the olfactory bulb and the dentate gyrus, respectively. Interestingly, convincing data has shown that brain insult invokes neurogenesis in various brain regions, such as the hippocampal cornu ammonis region, striatum, and cortex. These reports suggest that neural stem cells/neural progenitor cells, which can be activated by brain injury, might be broadly located in the adult brain or that new neurons may migrate widely from the neurogenic regions. This review focuses on brain insult-induced neurogenesis in the mammalian forebrain, especially in the neocortex.

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Abbreviations

BrdU:

Bromodeoxyuridine

CA:

Cornu ammonis

L1-INP:

Layer 1 inhibitory neuron progenitor

MGE:

Medial ganglionic eminence

NSC:

Neural stem cell

NPC:

Neural progenitor cell

SGZ:

Subgranular zone

SVZ:

Subventricular zone

References

  1. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1:67–73

    PubMed  CAS  Google Scholar 

  2. Rakic P (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 3:65–71

    PubMed  CAS  Google Scholar 

  3. Gage FH (2000) Mammalian Neural Stem Cells. Science 287:1433–1438

    PubMed  CAS  Google Scholar 

  4. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523–569

    PubMed  CAS  Google Scholar 

  5. Ming G, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250

    PubMed  CAS  Google Scholar 

  6. Rochefort C, Gheusi G, Vincent J, Lledo P (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679–2689

    PubMed  CAS  Google Scholar 

  7. Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010) Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J 24:2355–2363

    PubMed  CAS  Google Scholar 

  8. Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355–362

    PubMed  CAS  Google Scholar 

  9. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153–1161

    PubMed  CAS  Google Scholar 

  10. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29:13532–13542

    PubMed  CAS  Google Scholar 

  11. Kokaia Z, Lindvall O (2003) Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 13:127–132

    PubMed  CAS  Google Scholar 

  12. Palmer TD, Ray J, Gage FH (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6:474–486

    PubMed  CAS  Google Scholar 

  13. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716

    PubMed  CAS  Google Scholar 

  14. Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061

    PubMed  CAS  Google Scholar 

  15. Doetsch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 93:14895–14900

    PubMed  CAS  Google Scholar 

  16. Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981

    PubMed  CAS  Google Scholar 

  17. Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351–2358

    PubMed  CAS  Google Scholar 

  18. Duan X, Kang E, Liu CY, Ming G, Song H (2008) Development of neural stem cell in the adult brain. Curr Opin Neurobiol 18:108–115

    PubMed  CAS  Google Scholar 

  19. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    PubMed  CAS  Google Scholar 

  20. Ge S, Sailor KA, Ming G, Song H (2008) Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol 586:3759–3765

    PubMed  CAS  Google Scholar 

  21. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431–1568

    PubMed  CAS  Google Scholar 

  22. Raichle ME (1983) The pathophysiology of brain ischemia. Ann Neurol 13:2–10

    PubMed  CAS  Google Scholar 

  23. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768–7778

    PubMed  CAS  Google Scholar 

  24. Bernabeu R, Sharp FR (2000) NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab 20:1669–1680

    PubMed  CAS  Google Scholar 

  25. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710–4715

    PubMed  CAS  Google Scholar 

  26. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50:602–611

    PubMed  CAS  Google Scholar 

  27. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa K, Miyata T, Okano H, Hori M, Matsumoto M (2001) Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32:1890–1896

    PubMed  CAS  Google Scholar 

  28. Arvidsson A, Kokaia Z, Lindvall O (2001) N-methyl-d-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 14:10–18

    PubMed  CAS  Google Scholar 

  29. Zhang R, Wang Y, Zhang L, Zhang Z, Tsang W, Lu M, Zhang L, Chopp M (2002) Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33:2675–2680

    PubMed  CAS  Google Scholar 

  30. Takasawa K, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, Matsushita K, Ohstuki T, Miyata T, Okano H, Hori M, Matsumoto M (2002) Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 22:299–307

    PubMed  Google Scholar 

  31. Iwai M, Sato K, Omori N, Nagano I, Manabe Y, Shoji M, Abe K (2002) Three steps of neural stem cells development in gerbil dentate gyrus after transient ischemia. J Cereb Blood Flow Metab 22:411–419

    PubMed  CAS  Google Scholar 

  32. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53:743–751

    PubMed  CAS  Google Scholar 

  33. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, Greenberg DA (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111:1843–1851

    PubMed  CAS  Google Scholar 

  34. Zhu DY, Liu SH, Sun HS, Lu YM (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23:223–229

    PubMed  CAS  Google Scholar 

  35. Tonchev AB, Yamashima T, Zhao L, Okano HJ, Okano H (2003) Proliferation of neural and neuronal progenitors after global brain ischemia in young adult macaque monkeys. Mol Cell Neurosci 23:292–301

    PubMed  CAS  Google Scholar 

  36. Jin K, Sun Y, Xie L, Childs J, Mao XO, Greenberg DA (2004) Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 24:399–408

    PubMed  Google Scholar 

  37. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M (2004) Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35:1732–1737

    PubMed  CAS  Google Scholar 

  38. Kawai T, Takagi N, Miyake-Takagi K, Okuyama N, Mochizuki N, Takeo S (2004) Characterization of BrdU-positive neurons induced by transient global ischemia in adult hippocampus. J Cereb Blood Flow Metab 24:548–555

    PubMed  Google Scholar 

  39. Zhu DY, Lau L, Liu SH, Wei JS, Lu YM (2004) Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 101:9453–9457

    PubMed  CAS  Google Scholar 

  40. Komitova M, Mattsson B, Johansson BB, Eriksson PS (2005) Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 36:1278–1282

    PubMed  Google Scholar 

  41. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36:1790–1795

    PubMed  Google Scholar 

  42. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823–826

    PubMed  CAS  Google Scholar 

  43. Kobayashi T, Ahlenius H, Thored P, Kobayashi R, Kokaia Z, Lindvall O (2006) Intracerebral infusion of glial cell line-derived neurotrophic factor promotes striatal neurogenesis after stroke in adult rats. Stroke 37:2361–2367

    PubMed  CAS  Google Scholar 

  44. Koketsu D, Furuichi Y, Maeda M, Matsuoka N, Miyamoto Y, Hisatsune T (2006) Increased number of new neurons in the olfactory bulb and hippocampus of adult non-human primates after focal ischemia. Exp Neurol 199:92–102

    PubMed  Google Scholar 

  45. Macas J, Nern C, Plate KH, Momma S (2006) Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26:13114–13119

    PubMed  CAS  Google Scholar 

  46. Leker RR, Soldner F, Velasco I, Gavin DK, Androutsellis-Theotokis A, McKay RD (2007) Long-lasting regeneration after ischemia in the cerebral cortex. Stroke 38:153–161

    PubMed  Google Scholar 

  47. Liu XS, Zhang ZG, Zhang RL, Gregg S, Morris DC, Wang Y, Chopp M (2007) Stroke induces gene profile changes associated with neurogenesis and angiogenesis in adult subventricular zone progenitor cells. J Cereb Blood Flow Metab 27:564–574

    PubMed  CAS  Google Scholar 

  48. Suzuki S, Gerhold LM, Böttner M, Rau SW, Dela Cruz C, Yang E, Zhu H, Yu J, Cashion AB, Kindy MS, Merchenthaler I, Gage FH, Wise PM (2007) Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol 500:1064–1075

    PubMed  CAS  Google Scholar 

  49. Wang Y, Jin K, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA (2007) VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J Neurosci Res 85:740–747

    PubMed  CAS  Google Scholar 

  50. Lu L, Tonchev AB, Kaplamadzhiev DB, Boneva NB, Mori Y, Sahara S, Ma D, Nakaya MA, Kikuchi M, Yamashita T (2008) Expression of matrix metalloproteinases in the neurogenic niche of the adult monkey hippocampus after ischemia. Hippocampus 18:1074–1084

    PubMed  CAS  Google Scholar 

  51. Wang L, Chopp M, Zhang R, Zhang L, LeTourneau Y, Feng YF, Jiang A, Morris DC, Zhang ZG (2009) The Notch pathway mediates expansion of a progenitor pool and neuronal differentiation in adult neural progenitor cells after stroke. Neuroscience 158:1356–1363

    PubMed  CAS  Google Scholar 

  52. Wang X, Mao X, Xie L, Greenberg DA, Jin K (2009) Involvement of Notch1 signaling in neurogenesis in the subventricular zone of normal and ischemic rat brain in vivo. J Cereb Blood Flow Metab 29:1644–1654

    PubMed  Google Scholar 

  53. Tian H, Huang B, Zhao J, Hu X, Guo J, Li LX (2009) Non-receptor tyrosine kinase Src is required for ischemia-stimulated neuronal cell proliferation via Raf/ERK/CREB activation in the dentate gyrus. BMC Neurosci 10:139

    PubMed  Google Scholar 

  54. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, Martinez-Ramirez S, Jimenez-Xarrie E, Marín R, Martí-Vilalta JL, García-Verdugo JM (2010) Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 74:357–365

    PubMed  CAS  Google Scholar 

  55. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970

    PubMed  CAS  Google Scholar 

  56. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802–813

    PubMed  Google Scholar 

  57. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA (2003) Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24:171–189

    PubMed  CAS  Google Scholar 

  58. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O (2006) Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739–747

    PubMed  CAS  Google Scholar 

  59. Yamashita T, Ninomiya M, Hernández Acosta P, García-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K (2006) Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26:6627–6636

    PubMed  CAS  Google Scholar 

  60. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K (2010) Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 28:545–554

    PubMed  Google Scholar 

  61. Buchholtz A (1890) Ueber das Vorkommen von Karyokinesen in Zellen des Centralnervensystems von neugeborenen und jungen Hunden u. Kaninchen. Neurol Centralbl 9:140–142

    Google Scholar 

  62. Sclavunos G (1899) Ueber Keimzellen in d. weissen Substanz d. Ruckenmarks von alteren Embryonen und Neugeborenen. Anat Anz 16:467–473

    Google Scholar 

  63. Hamilton A (1901) The division of differentiated cells in the central nervous system of the white rat. J Comp Neurol 11:297–320

    Google Scholar 

  64. Allen E (1912) The cessation of mitosis in the central nervous system of the albino rat. J Comp Neurol 22:547–568

    Google Scholar 

  65. Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573–591

    PubMed  CAS  Google Scholar 

  66. Kaplan MS (1981) Neurogenesis in the 3-month-old rat visual cortex. J Comp Neurol 195:323–338

    PubMed  CAS  Google Scholar 

  67. Rakic P (1974) Neurons in rhesus visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425–427

    PubMed  CAS  Google Scholar 

  68. Rakic P (1982) Early developmental events: cell lineages, acquisition of neuronal positions, and areal and laminar development. Neurosci Res Program Bull 20:439–451

    PubMed  CAS  Google Scholar 

  69. Rakic P (1985) Limits of neurogenesis in primates. Science 227:1054–1056

    PubMed  CAS  Google Scholar 

  70. Cameron HA, Dayer AG (2008) New interneurons in the adult neocortex: small, sparse, but significant? Biol Psychiatry 63:650–655

    PubMed  Google Scholar 

  71. Gould E, Reeves AJ, Graziano MSA, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552

    PubMed  CAS  Google Scholar 

  72. Gould E, Vail N, Wagers M, Gross CG (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910–10917

    PubMed  CAS  Google Scholar 

  73. Bernier PJ, Bédard A, Vinet J, Lévesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99:11464–11469

    PubMed  CAS  Google Scholar 

  74. Koketsu D, Mikami A, Miyamoto Y, Hisatsune T (2003) Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 23:937–942

    PubMed  CAS  Google Scholar 

  75. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168:415–427

    PubMed  CAS  Google Scholar 

  76. Kimura K, Shimizu K, Hayashi M, Ishikawa T, Ago Y (2000) Pituitary–adrenocortical responses to the first dyadic encounters in male rhesus monkeys: effect of dominance relationship. Am J Primatol 50:247–256

    PubMed  CAS  Google Scholar 

  77. Kozorovitskiy Y, Gould E (2004) Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J Neurosci 24:6755–6759

    PubMed  CAS  Google Scholar 

  78. Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135:1127–1128

    PubMed  CAS  Google Scholar 

  79. Altman J (1966) Autoradiographic and histological studies of postnatal neurogenesis. II. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in infant rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 128:431–473

    Google Scholar 

  80. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951–955

    PubMed  CAS  Google Scholar 

  81. Gu W, Brannstrom T, Wester P (2000) Cortical neurogenesis in adult rats after reversible photothrombotic stroke. J Cereb Blood Flow Metab 20:1166–1173

    PubMed  CAS  Google Scholar 

  82. Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294:2127–2130

    PubMed  CAS  Google Scholar 

  83. Jiang W, Gu W, Brannstrom T, Rosqvist R, Wester P (2001) Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32:1201–1207

    PubMed  CAS  Google Scholar 

  84. Zhang RL, Zhang ZG, Zhang L, Chopp M (2001) Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105:33–41

    PubMed  CAS  Google Scholar 

  85. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99:11464–11469

    PubMed  CAS  Google Scholar 

  86. Ehninger D, Kempermann G (2003) Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 13:845–851

    PubMed  Google Scholar 

  87. Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G II, Jiang L, Kang J, Nedergaard M, Goldman SA (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439–447

    PubMed  CAS  Google Scholar 

  88. Chen J, Magavi SSP, Macklis JD (2004) Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci USA 101:16357–16362

    PubMed  CAS  Google Scholar 

  89. Tonchev AB, Yamashima T, Sawamoto K, Okano H (2005) Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia. J Neurosci Res 81:776–788

    PubMed  CAS  Google Scholar 

  90. Sundholm-Peters NL, Yang HKC, Goings GE, Walker AS, Szele FG (2005) Subventricular zone neuroblasts emigrate toward cortical lesions. J Neuropathol Exp Neurol 64:1089–1100

    PubMed  Google Scholar 

  91. Takemura N (2005) Evidence for neurogenesis within the white matter beneath the temporal neocortex of the adult rat brain. Neuroscience 134:121–132

    PubMed  CAS  Google Scholar 

  92. Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Björk-Eriksson T, Nordborg C, Gage FH, Druid H, Eriksson PS, Frisén J (2006) Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci USA 103:12564–12568

    PubMed  CAS  Google Scholar 

  93. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci USA 103:13198–13202

    PubMed  CAS  Google Scholar 

  94. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H (2007) Multi-directional differentiation of doublecortin- and NG2-immunopositive progenitor cells in the adult rat neocortex in vivo. Eur J Neurosci 25:3489–3498

    PubMed  Google Scholar 

  95. Li W, Yu SP, Ogle ME, Ding XS, Wei L (2008) Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice. Dev Neurobiol 68:1474–1486

    PubMed  CAS  Google Scholar 

  96. Sirko S, Neitz A, Mittmann T, Horvat-Bröcker A, von Holst A, Eysel UT, Faissner A (2009) Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain 132:2252–2264

    PubMed  Google Scholar 

  97. Xue J, Yanamoto H, Nakajo Y, Tohnai N, Nakano Y, Hori T, Iihara K, Miyamoto S (2009) Induced spreading depression evokes cell division of astrocytes in the subpial zone, generating neural precursor-like cells and new immature neurons in the adult cerebral cortex. Stroke 40:e606–e613

    PubMed  Google Scholar 

  98. Nakayama D, Matsuyama T, Ishibashi-Ueda H, Nakagomi T, Kasahara Y, Hirose H, Kikuchi-Taura A, Stern DM, Mori H, Taguchi A (2010) Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur J Neurosci 31:90–98

    PubMed  Google Scholar 

  99. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, Miyakawa T, Kaneko T, Nakamura S (2010) Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci 13:173–179

    PubMed  CAS  Google Scholar 

  100. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M (2008) Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28:10434–10442

    PubMed  CAS  Google Scholar 

  101. Komitova M, Zhu X, Serwanski DR, Nishiyama A (2009) NG2 cells are distinct from neurogenic cells in the postnatal mouse subventricular zone. J Comp Neurol 512:702–716

    PubMed  Google Scholar 

  102. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9–22

    PubMed  CAS  Google Scholar 

  103. Platel J, Gordon V, Heintz T, Bordey A (2009) GFAP–GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 57:66–78

    PubMed  Google Scholar 

  104. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, Gallo V (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161:169–186

    PubMed  CAS  Google Scholar 

  105. Aguirre A, Gallo V (2004) Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci 24:10530–10541

    PubMed  CAS  Google Scholar 

  106. Aguirre AA, Chittajallu R, Belachew S, Gallo V (2004) NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J Cell Biol 165:575–589

    PubMed  CAS  Google Scholar 

  107. Ohira K, Kaneko T (2010) Injection of virus vectors into the neocortical layer 1. Nat Protoc. doi:10.1038/nproc.2010.21

  108. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612–2622

    PubMed  CAS  Google Scholar 

  109. Cobos I, Long JE, Thwin MT, Rubenstein JL (2006) Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex 16:i82–i88

    PubMed  Google Scholar 

  110. Costa MR, Kessaris N, Richardson WD, Gotz M, Hedin-Pereira C (2007) The marginal zone/layer I as a novel niche for neurogenesis and gliogenesis in developing cerebral cortex. J Neurosci 27:11376–11388

    PubMed  CAS  Google Scholar 

  111. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881–7888

    PubMed  CAS  Google Scholar 

  112. Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619

    PubMed  CAS  Google Scholar 

  113. Jiménez D, Rivera R, López-Mascaraque L, De Carlos JA (2003) Origin of the cortical layer I in rodents. Dev Neurosci 25:105–115

    PubMed  Google Scholar 

  114. Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176

    PubMed  CAS  Google Scholar 

  115. Marin O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26:441–483

    PubMed  CAS  Google Scholar 

  116. Kroll TT, O’Leary DDM (2005) Ventralized dorsal telencephalic progenitors in Pax6 mutant mice generate GABA interneurons of a lateral ganglionic eminence fate. Proc Natl Acad Sci USA 102:7374–7379

    PubMed  CAS  Google Scholar 

  117. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706–6717

    PubMed  CAS  Google Scholar 

  118. Bédard A, Cossette M, Lévesque M, Parent A (2002) Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci Lett 328:213–216

    PubMed  Google Scholar 

  119. Luzzati F, De Marchis S, Fasolo A, Peretto P (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26:609–621

    PubMed  CAS  Google Scholar 

  120. Keilhoff G, Becker A, Grecksch G, Bernstein H, Wolf G (2006) Cell proliferation is influenced by bulbectomy and normalized by imipramine treatment in a region-specific manner. Neuropsychopharmacology 31:1165–1176

    PubMed  CAS  Google Scholar 

  121. Arsenijevic Y, Villemure JG, Brunet JF, Bloch JJ, Déglon N, Kostic C, Zurn A, Aebischer P (2001) Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp Neurol 170:48–62

    PubMed  CAS  Google Scholar 

  122. Fowler CD, Liu Y, Ouimet C, Wang Z (2002) The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115–128

    PubMed  Google Scholar 

  123. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429–441

    PubMed  CAS  Google Scholar 

  124. Huang L, DeVries GJ, Bittman EL (1998) Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J Neurobiol 36:410–420

    PubMed  CAS  Google Scholar 

  125. Kokoeva MV, Yin H, Flier JS (2005) Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310:679–683

    PubMed  CAS  Google Scholar 

  126. Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y, Matsumoto N, Dezawa M, Ide C (2005) Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192:251–264

    PubMed  CAS  Google Scholar 

  127. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisén J, Janson AM (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 100:7925–7930

    PubMed  CAS  Google Scholar 

  128. Ponti G, Peretto P, Bonfanti L (2006) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294:168–180

    PubMed  CAS  Google Scholar 

  129. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16:7599–7609

    PubMed  CAS  Google Scholar 

  130. Kehl LJ, Fairbanks CA, Laughlin TM, Wilcox GL (1997) Neurogenesis in postnatal rat spinal cord: a study in primary culture. Science 276:586–589

    PubMed  CAS  Google Scholar 

  131. Shihabuddin LS, Ray J, Gage FH (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148:577–586

    PubMed  CAS  Google Scholar 

  132. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisén J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34

    PubMed  CAS  Google Scholar 

  133. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:2218–2228

    PubMed  CAS  Google Scholar 

  134. Shihabuddin LS, Horner PJ, Ray J, Gage FH (2000) Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 20:8727–8735

    PubMed  CAS  Google Scholar 

  135. Bédard A, Lévesque M, Bernier PJ, Parent A (2002) The rostral migratory stream in adult squirrel monkeys: contribution of new neurons to the olfactory tubercle and involvement of the antiapoptotic protein Bcl-2. Eur J Neurosci 16:1917–1924

    PubMed  Google Scholar 

  136. Pekcec A, Löscher W, Potschka H (2006) Neurogenesis in the adult rat piriform cortex. Neuroreport 17:571–574

    PubMed  Google Scholar 

  137. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488

    PubMed  CAS  Google Scholar 

  138. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P (2004) No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 101:10177–10182

    PubMed  CAS  Google Scholar 

  139. Cooper O, Isacson O (2004) Intrastriatal transforming growth factor alpha delivery to a model of Parkinson’s disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 24:8924–8931

    PubMed  CAS  Google Scholar 

  140. Weissman IL (2000) Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science 287:1442–1446

    PubMed  CAS  Google Scholar 

  141. Donovan PJ, Gearhart J (2001) The end of the beginning for pluripotent stem cells. Nature 414:92–97

    PubMed  CAS  Google Scholar 

  142. Selvaraj V, Plane JM, Williams AJ, Deng W (2010) Switching cell fate: the remarkable rise of induced pluripotent stem cells and lineage reprogramming technologies. Trends Biotechnol 28:214–223

    PubMed  CAS  Google Scholar 

  143. Okita K, Yamanaka S (2010) Induction of pluripotency by defined factors. Exp Cell Res 316:2565–2570

    PubMed  CAS  Google Scholar 

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Acknowledgments

I thank Dr. Greta Anderson for critical reading of the manuscript. This work was supported by the Ministry of Education, Culture, Sports, Science and Technology, Grants-in-Aid for Young Scientists (B), 21700384.

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Correspondence to Koji Ohira.

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Ohira, K. Injury-induced neurogenesis in the mammalian forebrain. Cell. Mol. Life Sci. 68, 1645–1656 (2011). https://doi.org/10.1007/s00018-010-0552-y

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