Neuroblasts of the postnatal mammalian forebrain: Their phenotype and fate

Journal of Neurobiology

Volumn 36, Issue 2, 1998, Pages 221-233

  Luskin, Marla B ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Migration; Olfactory bulb; Progenitor cell; Proliferation; Transplantation

Indexed keywords

BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN VENTRICLE; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CORPUS STRIATUM; FOREBRAIN; GERM LAYER; GLIA CELL; INTERNEURON; NEUROBLAST; NEWBORN; NONHUMAN; OLFACTORY BULB; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANIMALS, NEWBORN; CELL LINE; NEURONS; OLFACTORY BULB; PHENOTYPE; PROSENCEPHALON; STEM CELLS;

EID: 0031927325     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199808)36:2<221::AID-NEU9>3.0.CO;2-3     Document Type: Review

References (75)

1. ALTMAN, J. (1969). Autoradiographic and histological studies of postnatal neurogenesis IV: cell proliferation and migration in the anterior forebrain. with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137:433-458.
2. ALTMAN, J. and DAS, G. D. (1966). Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 127:337-390.
3. BAKER, H. and FARBMAN, A. I. (1993). Olfactory afferent regulation of the dopamine phenotype in the fetal rat olfactory system. Neuroscience 52:115-134.
4. BARKER, R. A., DUNNETT, S. B., FAISSNER, A., and FAWCETT, J. W. (1996). The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp. Neurol. 141:79-93.
5. 3H-Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50:329-340.
6. BERNHARDT, R. and MATUS, A. (1984). Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeletons. J. Comp. Neurol. 226:203-221.
7. BETARBET, R., ZIGOVA, T., BAKAY, R. A. E., and LUSKIN, M. B. (1996). Migration patterns of neonata subventricular zone progenitor cells transplanted into the neonatal striatum. Cell Transplant. 5:165-178.
8. Boulder Committee (1970). Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166:257-261.
9. CREMER, H., LANGE, R., CHRISTOPH, A., PLOMANN, M., VOPPER, G., ROES, J., BROWN, R., BALDWIN, S., KRAEMER, P., SCHEFF, S., BATHELS, D., RAJEWSKY, K., and WILLE, W. (1994). Inactivation of the NCAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
10. DAVIS, A. A. and TEMPLE, A. (1994). A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372:263-266.
11. DICICCO-BLOOM, E., TOWNES-ANDERSON, E., and BLACK, E. B. (1990). Neuroblast mitosis in dissociated culture: regulation and relationship to differentiation. J. Cell Biol. 110:2073-2086.
12. DOETSCH, F., GARCIA-VERDUGO, J. M., and ALVAREZ-BUYLLA, A. (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. Neuroscience 17:5046-5061.
13. EASTER, S., ROSS, L., and FRANKFURTER, A. (1993). Initial tract formation in the mouse brain. J. Neurosci. 13:285-299.
14. FARBMAN, A. I. (1991). Developmental neurobiology of the olfactory system. In: Smell and Taste in Health and Disease. T. Getchell, R. Doty, L. Bartoshuk, and J. Snow, Eds. Raven, New York, pp. 19-33.
15. FRAZIER-CIERPIAL, L. and BRUNJES, P. (1989). Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats. J. Comp. Neurol. 289:481-492.
16. GAGE, F. H., RAY, J., and FISHER, L. J. (1995). Isolation, characterization, and use of stem cells from the CNS. Annu. Rev. Neurosci. 18:159-192.
17. GARCÍA-VERDUGO, J. M., DOETSCH, F., WICHTERLE, H., LIM, D. A., and ALVAREZ-BUYLLA, A. (1998). The SVZ: a source of stem cells in the adult brain. J. Neurobiol. 36:234-248.
18. GOLDMAN, S., KIRSCHENBAUM, B., HARRISON-RESTELLI, C., and THALER, H. (1997). Neuronal precursor cells of the adult rat ventricular zone persist into senescence, with no change in spatial extent or BDNF response. J. Neurobiol. 32:554-566.
19. GOLDMAN, S. A. (1990). Neuronal development and migration in explant cultures of the adult canary forebrain. J. Neurosci. 10:2931-2939.
20. GOLDMAN, S. A. (1995). Neuronal precursor cells and neurogenesis in the adult forebrain. Neuroscientist 1:338-350.
21. GOLDMAN, S. A., and LUSKIN, M. B. (1998). Strategies utilized by migrating neurons of the postnatal vertebrate forebrain. Trends Neurosci. 21:107-114.
22. GOLDMAN, S. A. and NOTTEBOHM, F. (1983). Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. 80:2390-2394.
23. GOLDMAN, S. A., ZAREMBA, A., and NIEDZWIECKI, D. (1992). In vitro neurogenesis by neuronal precursor cells derived from the adult songbird brain. J. Neurosci. 12:2532-2541.
24. HINDS, J. W. (1968a). Autoradiographic study of histogenesis in the mouse olfactory bulb I: time of origin of neurons and neuroglia. J. Comp. Neurol. 134:287-304.
25. HINDS, J. W. (1968b). Autoradiographic study of histogenesis in the mouse olfactory bulb II: cell proliferation and migration. J. Comp. Neurol. 134:305-322.
26. Hu, H. and RUTISHAUSER, U. (1996). A septum derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16:933-940.
27. JANKOVSKI, A., ROSSI, F., and SOTELO, C. (1996). Neuronal precursors in the postnatal mouse cerebellum are fully committed cells: evidence from heterochronic transplantations. Eur. J. Neurosci. 8:2308-2319.
28. JANKOVSKI, A. and SOTELO, C. (1996). Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotropic transplantation. J. Comp. Neurol. 371:376-396.
29. KIRSCHENBAUM, B. and GOLDMAN, S. A. (1995). Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. 92:210-214.
30. KIRSCHENBAUM, B., NEDERGAARD, M., PREUSS, A., BARAMI, K., FRASER, R. A., and GOLDMAN, S. A. (1994). In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cerebral Cortex 4:576-589.
31. KISHI, K. (1987). Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J. Comp. Neurol. 258:112-124.
32. KISHI, K., PENG, J., KAKUTA, S., MURAKAMI, K., KURODA, M., YOKOTA, S., HAYAKAWA, S., KUGE, T., and ASAYAMA, T. (1990). Migration of bipolar supendymal cells, precursors of the granule cells of the rat olfactory bulb, with reference to the arrangement of the radial glial fibers. Arch. Histol. Cytol. 53:219-226.
33. LEE, M., REBHUN, L., and FRANKFURTER, A. (1990). Posttranslational modification of class ni β-tubulin. Proc. Natl. Acad. Sci. 87:7195-7199.
34. LEVINE, S. M. and GOLDMAN, J. E. (1988). Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J. Neurosci. 8:3992-4006.
35. LEVISON, S. and GOLDMAN, J. E. (1997). Multipotential and lineage-restricted precursors coexist in the mammalian perinatal subventricular zone. J. Neurosci. Res. 48:83-94.
36. LOIS, C. and ALVAREZ-BUYLLA, A. (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. 90:2074-2077.
37. LOIS, C. and ALVAREZ-BUYLLA, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
38. LOIS, C., GARCIA-VERDUGO, J. M., and ALVAREZ-BUYLLA, A. (1996). Chain migration of neuronal precursors. Science 271:978-981.
39. LUSKIN, M. B., ZIGOVA, T., SOTERES, B. S., and STEWART, R. R. (1997). Neuronal progenitor cells derived from the anterior subventricular zone of the neonatal rat forebrain continue to proliferate in vitro and express a neuronal phenotype. Mol. Cell. Neurosci. 8:351-366.
40. LUSKIN, M. B. (1993a). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
41. LUSKIN, M. B. (1993b). Mammalian forebrain development: how cells find a permanent home and establish their identity. J. NIH Res. 5:60-64.
42. LUSKIN, M. B. and BOONE, M. S. (1994). Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses 19:695-714.
43. LUSKIN, M. B. and MCDERMOTT, K. (1994). Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 11:211-226.
44. MCCONNELL, S. K. (1988). Development and decision-making in the mammalian cerebral cortex. Brain Res. Rev. 13:1-23.
45. MEMBERG, S. P. and HALL, A. K. (1995). Dividing neuron precursors express neuron-specific tubulin. J. Neurobiol. 27:26-43.
46. MENEZES, J. R. and LUSKIN, M. B. (1994). Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 14:5399-5416.
47. MENEZES, J. R., SMITH, C. M., NELSON, K. C. and LUSKIN, M. B. (1995). The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6:496-508.
48. MIRAGALL, F., KADMON, G., FAISSNER, A., ANTONICEK, H., and SCHACHNER, M. (1990). Retention of J1/tenascin and the polysialylated form of the neural cell adhesion molecule (N-CAM) in the adult olfactory bulb. J. Neurocytol. 19:899-914.
49. MORSHEAD, C. and VAN DER KOOY, D. (1992). Postmitotic death is the fate of constituitively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12:249-256.
50. MORSHEAD, C. M., REYNOLDS, B. A., CRAIG, C. G., MCBURNEY, M. W., STAINES, W. A., MORASSUTTI, D., WEISS, S., and VAN DER KOOY, D. (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
51. NOBLE, M., WREN, D., and WOLSWIJK, G. (1992). The O-2A (adult) progenitor cells: a glial stem cell of the adult central nervous system. Semin. Cell Biol. 3:413-422.
52. ONO, K., TOMASIEWICZ, H., MAGNUSON, T., and RUTISHAUSER, U. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13:595-609.
53. PALMER, T. D., RAY, J., and GAGE, F. H. (1995). FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6:474-486.
54. PRIVAT, A. (1975). Postnatal gliogenesis in the mammalian brain. Int. Rev. Cytol. 40:281-323.
55. RAEDLER, E. and RAEDLER, A. (1978). Autoradiographic study of early neurogenesis in rat cerebral cortex. Anat. Embryol. 154:267-312.
56. RAKIC, P. (1990). Principles of neural cell migration. Experientia 46:882-891.
57. RAKIC, P. (1971). Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33:471-476.
58. REYNOLDS, B. A. and WEISS, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
59. RICHARDS, L. J., KILPATRICK, T. J., and BARTLETT, P. F. (1992). De novo generation of neuronal cells from the adult mouse brain. Proc. Nail. Acad. Sci. 89:8591-8595.
60. ROUSSELOT, P., LOIS, C., and ALVAREZ-BUYLLA, A. (1994). Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351:51-61.
61. SEKI, T. and ARAI, Y. (1993). Distribution and possible roles of the polysialated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res. 17:265-290.
62. SKOFF, R. P. (1980). Neuroglia: a reevaluation of their origin and development. Pathol Res. Pract. 168:279-300.
63. SMART, I. (1961). The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine injection. J. Comp. Neurol. 116:325-347.
64. SNYDER, E. Y., DEITHER, D. L., WALSH, C., ARNOLD-ALDEA, S., HARTWIEG, E. A., and CEPKO, C. L. (1992). Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 69:33-51.
65. SNYDER, E. Y., PARK, K. I., FLAX, J. D., LIU, S., ROSARIO, C. M., YANDAVE, B. D., and AURORA, S. (1997). Potential of neural "stem-like" cells for gene therapy and repair of the degenerating central nervous system. Adv. Neurol. 72:121-132.
66. SUHONEN, J., PETERSON, D., RAY, J., and GAGE, F. (1996). Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383:624-627.
67. THOMAS, L. B., GATES, M., and STEINDLER, D. A. (1996). Young neurons from the adult subependymal zone proliferate and migrate along astrocyte. extracellular matrix-rich pathway. Glia 17:1-14.
68. VAYSSE, P. and GOLDMAN, J. (1990). A clonal analysis of glia lineages in neonatal forebrain development in vitro. Neuron 5:227-235.
69. VESCOVI, A. L., REYNOLDS, B. A., FRASER, D. D., and WEISS, S. (1993). bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11:951-966.
70. WEISS, S. and VAN DER KOOY, D. (1998). CNS stem cells - where's the biology (a.k.a. beef)? J. Neurobiol. 36:307-314.
71. WHITTEMORE, S. R., EATON, M. J., and ONIFER. S. M. (1997). Gene therapy and the use of stem cells for central nervous system regeneration. Adv. Neurol. 72:113-119.
72. WICHTERLE, H., GARCIA-VERDUGO, J., and ALVAREZ-BUYLLA, A. (1997). Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18:779-791.
73. ZIGOVA, T., BETARBET, R., SOTERES, B. J., BROCK, S., BAKAY, R. A., and LUSKIN, M. B. (1996). A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted telencephalic ventricular zone cells. Dev. Biol. 173:459-474.
74. ZIGOVA, T., PENCEA, V., BETARBET, R., WIEGAND, S. J., ALEXANDER, C., BAKAY, R. A., and LUSKIN, M. B. (1998). Neuronal progenitor cells of the neonatal sub-ventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant. 7:137-156.
75. ZIGOVA, T., PENCEA, V., WIEGAND, S. J., and LUSKIN, M. B. (1988). Intraventricular administration of BDNF increases the number of newly-generated neurons in the adult olfactory bulb. Mol. and Cell. Neurosci. (in press).