Endogenous Neurogenesis in Postnatal Brain

출생 후 뇌의 내인성 신경세포 생성

  • Chang, Yun Sil (Department of Pediatrics, Samsung Medical Center, Sungkyunkwan Universtiy School of Medicine)
  • 장윤실 (성균관대학교 의과대학 삼성서울병원 소아과)
  • Received : 2005.07.25
  • Accepted : 2005.07.27
  • Published : 2005.08.15

Abstract

Repair mechanisms in the postnatal and mature central nervous system(CNS) have long been thought to be very limited. However recent works have shown that the mature CSN contains neural progenitors, precursors, and stem cells that are capable of generating new neurons, astrocytes, and oligodendrocytes especially in germinative areas such as the subventricular zone of the lateral ventricles, the dentate gyrus of the hippocampus. These findings raise the possibilities for the development of novel neural repair strategies via mobilization and replacement for dying neurons of neural stem cells in situ. Indeed recent reports have provided evidences that endogenous stem cells are activated in response to various injuries, and in some injury models, limited neuronal replacement occurs in the CNS. Here, current understandings for endogenous neurogenesis and induction neurogeneis in postnatal CNS including neonatal brain are summarized and discussed.

Keywords

References

  1. Gage FH. Mammalian neural stem cells. Science 2000;287: 1433-8 https://doi.org/10.1126/science.287.5457.1433
  2. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124:319-35 https://doi.org/10.1002/cne.901240303
  3. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-10 https://doi.org/10.1126/science.1553558
  4. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002;69:745-9 https://doi.org/10.1002/jnr.10378
  5. Allen E. The cessation of mitosis in the central nervous system of the albino rat. J Comp Neurol 1912;22:537-68
  6. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci USA 2000;97:1823-8 https://doi.org/10.1073/pnas.97.4.1823
  7. Cameron HA, Woolley CS, McEwen BS, Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993;56:337-44 https://doi.org/10.1016/0306-4522(93)90335-D
  8. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat : age-related decrease of neuronal progenitor proliferation. J Neurosci 1996;16:2027- 33
  9. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002;415:1030-4 https://doi.org/10.1038/4151030a
  10. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 2003;460:563-72 https://doi.org/10.1002/cne.10675
  11. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates. Science 1999;286: 548-52 https://doi.org/10.1126/science.286.5439.548
  12. Rietze R, Poulin P, Weiss S. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J Comp Neurol 2000;424:397-408 https://doi.org/10.1002/1096-9861(20000828)424:3<397::AID-CNE2>3.0.CO;2-A
  13. Bauer S, Hay M, Amilhon B, Jean A, Moyse E. In vivo neurogenesis in the dorsal vagal complex of the adult rat brainstem. Neuroscience 2005;130:75-90 https://doi.org/10.1016/j.neuroscience.2004.08.047
  14. Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M. Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol 2001;172:115-27 https://doi.org/10.1006/exnr.2001.7798
  15. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 2002;99: 11464-9 https://doi.org/10.1073/pnas.172403999
  16. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, et al. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 2003;100:7925-30 https://doi.org/10.1073/pnas.1131955100
  17. Bedard A, Cossette M, Levesque M, Parent A. Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci Lett 2002;328:213-6 https://doi.org/10.1016/S0304-3940(02)00530-X
  18. Kornack DR, Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 2001;294:2127-30 https://doi.org/10.1126/science.1065467
  19. Koketsu D, Mikami A, Miyamoto Y, Hisatsune T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 2003;23:937-42
  20. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 2004;101: 10177-82 https://doi.org/10.1073/pnas.0401229101
  21. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000;425: 479-94 https://doi.org/10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3
  22. Yang Y, Mufson EJ, Herrup K. Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J Neurosci 2003;23:2557-63
  23. Kuan CY, Schloemer AJ, Lu A, Burns KA, Weng WL, Williams MT, et al. Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci 2004;24:10763-72 https://doi.org/10.1523/JNEUROSCI.3883-04.2004
  24. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 2003;6:507-18
  25. Tramontin AD, Garcia-Verdugo JM, Lim DA, Alvarez- Buylla A. Postnatal development of radial glia and the ventricular zone(VZ) : a continuum of the neural stem cell compartment. Cereb Cortex 2003;13:580-7 https://doi.org/10.1093/cercor/13.6.580
  26. Luskin MB. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993;11:173-89 https://doi.org/10.1016/0896-6273(93)90281-U
  27. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004;427:740-4. https://doi.org/10.1038/nature02301
  28. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez- Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-16 https://doi.org/10.1016/S0092-8674(00)80783-7
  29. Gritti A, Cova L, Parati EA, Galli R, Vescovi AL. Basic fibroblast growth factor supports the proliferation of epidermal growth factor-generated neuronal precursor cells of the adult mouse CNS. Neurosci Lett 1995;185:151-4 https://doi.org/10.1016/0304-3940(95)11247-T
  30. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, et al. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 1996;16:1091-100
  31. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez- Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002;36:1021-34 https://doi.org/10.1016/S0896-6273(02)01133-9
  32. Tropepe V, Craig CG, Morshead CM, van der Kooy D. Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 1997;17:7850-9
  33. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996;16:2649-58
  34. Wagner JP, Black IB, DiCicco-Bloom E. Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 1999; 19:6006-16
  35. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia- Verdugo JM, Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000;28:713-26 https://doi.org/10.1016/S0896-6273(00)00148-3
  36. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor(VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002;99:11946-50 https://doi.org/10.1073/pnas.182296499
  37. Zigova T, Pencea V, Wiegand SJ, Luskin MB. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 1998;11:234-45 https://doi.org/10.1006/mcne.1998.0684
  38. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. 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 2001;21:6706-17
  39. Cooper-Kuhn CM, Vroemen M, Brown J, Ye H, Thompson MA, Winkler J, et al. Impaired adult neurogenesis in mice lacking the transcription factor E2F1. Mol Cell Neurosci 2002;21:312-23 https://doi.org/10.1006/mcne.2002.1176
  40. Soria JM, Taglialatela P, Gil-Perotin S, Galli R, Gritti A, Verdugo JM, et al. Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J Neurosci 2004;24:11171-81 https://doi.org/10.1523/JNEUROSCI.3248-04.2004
  41. Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, et al. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 2001;68:141- 52 https://doi.org/10.1046/j.1432-0436.2001.680208.x
  42. Taupin P, Ray J, Fischer WH, Suhr ST, Hakansson K, Grubb A, et al. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 2000;28:385-97 https://doi.org/10.1016/S0896-6273(00)00119-7
  43. Shi Y, Chichung Lie D, Taupin P, Nakashima K, Ray J, Yu RT, et al. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 2004;427: 78-83 https://doi.org/10.1038/nature02211
  44. Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H, et al. Generalized potential of adult neural stem cells. Science 2000;288:1660-3 https://doi.org/10.1126/science.288.5471.1660
  45. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447-52 https://doi.org/10.1016/j.tins.2004.05.013
  46. Seki T, Arai Y. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 1995;6:2479-82 https://doi.org/10.1097/00001756-199512150-00010
  47. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998;95:3168-71 https://doi.org/10.1073/pnas.95.6.3168
  48. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999;2:260-5 https://doi.org/10.1038/6365
  49. Ra SM, Kim H, Jang MH, Shin MC, Lee TH, Lim BV, et al. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci Lett 2002;333:123-6 https://doi.org/10.1016/S0304-3940(02)01031-5
  50. Jessberger S, Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 2003;18:2707-12 https://doi.org/10.1111/j.1460-9568.2003.02986.x
  51. Palmer TD, Takahashi J, Gage FH. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 1997;8:389-404 https://doi.org/10.1006/mcne.1996.0595
  52. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 1999;96:5263-7 https://doi.org/10.1073/pnas.96.9.5263
  53. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999;156:333-44 https://doi.org/10.1006/exnr.1999.7028
  54. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998;4:1313-7. https://doi.org/10.1038/3305
  55. Kempermann G, Wiskott L, Gage FH. Functional significance of adult neurogenesis. Curr Opin Neurobiol 2004;14: 186-91 https://doi.org/10.1016/j.conb.2004.03.001
  56. Trejo JL, Carro E, Torres-Aleman I. Circulating insulinlike growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001;21:1628-34
  57. Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994;61: 203-9 https://doi.org/10.1016/0306-4522(94)90224-0
  58. Brezun JM, Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999;89:999-1002 https://doi.org/10.1016/S0306-4522(98)00693-9
  59. Szele FG, Chesselet MF. Cortical lesions induce an increase in cell number and PSA-NCAM expression in the subventricular zone of adult rats. J Comp Neurol 1996;368: 439-54 https://doi.org/10.1002/(SICI)1096-9861(19960506)368:3<439::AID-CNE9>3.0.CO;2-6
  60. Calza L, Giardino L, Pozza M, Bettelli C, Micera A, Aloe L. Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis : in vivo evidence of a role for nerve growth factor. Proc Natl Acad Sci USA 1998;95:3209-14 https://doi.org/10.1073/pnas.95.6.3209
  61. Parent JM, Lowenstein DH. Mossy fiber reorganization in the epileptic hippocampus. Curr Opin Neurol 1997;10:103-9 https://doi.org/10.1097/00019052-199704000-00006
  62. Liu J, Solway K, Messing RO, Sharp FR. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 1998;18:7768-78
  63. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana- Adalid V, Bachelin C, Van Evercooren AB. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 1999;11:4357-66 https://doi.org/10.1046/j.1460-9568.1999.00873.x
  64. Holmin S, Almqvist P, Lendahl U, Mathiesen T. Adult nestin-expressing subependymal cells differentiate to astrocytes in response to brain injury. Eur J Neurosci 1997;9: 65-75 https://doi.org/10.1111/j.1460-9568.1997.tb01354.x
  65. Alonso G, Prieto M, Chauvet N. Tangential migration of young neurons arising from the subventricular zone of adult rats is impaired by surgical lesions passing through their natural migratory pathway. J Comp Neurol 1999;405: 508-28 https://doi.org/10.1002/(SICI)1096-9861(19990322)405:4<508::AID-CNE5>3.0.CO;2-5
  66. Fallon J, Reid S, Kinyamu R, Opole I, Opole R, Baratta J, et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 2000;97:14686- 91 https://doi.org/10.1073/pnas.97.26.14686
  67. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature 2000;405: 951-5 https://doi.org/10.1038/35016083
  68. Gray WP, Sundstrom LE. Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res 1998;790:52-9 https://doi.org/10.1016/S0006-8993(98)00030-4
  69. Parent JM, Valentin VV, Lowenstein DH. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci 2002;22:3174-88
  70. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 2001;98:4710-5 https://doi.org/10.1073/pnas.081011098
  71. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002;8:963-70 https://doi.org/10.1038/nm747
  72. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 2002;52:802-13 https://doi.org/10.1002/ana.10393
  73. Parent JM. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 2003;9:261-72 https://doi.org/10.1177/1073858403252680
  74. Abrahams JM, Gokhan S, Flamm ES, Mehler MF. De novo neurogenesis and acute stroke : are exogenous stem cells really necessary? Neurosurgery 2004;54:150-6
  75. Suzuki SO, Goldman JE. Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways : a dynamic study of glial and neuronal progenitor migration. J Neurosci 2003;23:4240-50
  76. Levison SW, Rothstein RP, Romanko MJ, Snyder MJ, Meyers RL, Vannucci SJ. Hypoxia/ischemia depletes the rat perinatal subventricular zone of oligodendrocyte progenitors and neural stem cells. Dev Neurosci 2001;23:234-47 https://doi.org/10.1159/000046149
  77. Plane JM, Liu R, Wang TW, Silverstein FS, Parent JM. Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol Dis 2004;16:585-95 https://doi.org/10.1016/j.nbd.2004.04.003
  78. Chang YS, Mu D, Wendland M, Sheldon RA, Vexler ZS, McQuillen PS, et al. Erythropoietin improves functional and histological outcome in neonatal stroke. Pediatr Res 2005; 58:106-11 https://doi.org/10.1203/01.PDR.0000163616.89767.69
  79. Lie DC, Song H, Colamarino SA, Ming GL, Gage FH. Neurogenesis in the adult brain : new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 2004;44:399-421 https://doi.org/10.1146/annurev.pharmtox.44.101802.121631