The subependymal layer in rodents: A site of structural plasticity and cell migration in the adult mammalian brain

Brain Research Bulletin

Volumn 49, Issue 4, 1999, Pages 221-243

  Peretto, Paolo ^a   Merighi, Adalberto ^a   Fasolo, Aldo ^b   Bonfanti, Luca ^a  

^a And Department of ^*  (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Glia; Neurogenesis; Olfactory bulb; Stem cells; Subventricular zone

Indexed keywords

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ASTROCYTE; BRAIN; CELL MIGRATION; CELL PROLIFERATION; FOREBRAIN; GLIA CELL; HIPPOCAMPUS; NERVOUS SYSTEM DEVELOPMENT; NERVOUS TISSUE; NEUROEPITHELIUM; NONHUMAN; NOSE MUCOSA; OLFACTORY BULB; PERINATAL PERIOD; PLASTICITY; PRIORITY JOURNAL; RAT; REVIEW; STEM CELL;

ANIMALS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL DIVISION; CELL MOVEMENT; IMMUNOHISTOCHEMISTRY; MICE; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; PROSENCEPHALON; RATS;

EID: 0032814037     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(99)00037-4     Document Type: Review

References (184)

1. Abbott, N. J. Glial-neuronal interaction. Ann. N. Y. Acad. Sci. 633; 1991.
2. Altman J. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat. Rec. 145:1963;573-592.
3. Altman J. Autoradiographic and histological studies of postnatal neurogenesis, III Dating the time of production and onset of differentiation of cerebellar microneurons in rats . J. Comp. Neurol. 136:1969;269-294.
4. Altman J. 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. 137:1969;433-458.
5. Altman J., Bayer S.A. Transformation of the paired cerebellar primordia into the unified primitive cerebellum. Altman J., Bayer S.A. Development of the cerebellar system In relation to its evolution, structure and functions . 1997;138-169 C.R.C. Press, Boca Raton, FL.
6. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124:1965;319-336.
7. Alvarez-Buylla A. Neurogenesis in the adult brain Prospects for brain repair . Gage F.H., Christen Y. Isolation, characterization and utilization of CNS stem cells. 1997;86-100 Springer-Verlag, Berlin.
8. Alvarez-Buylla A., Buskirk D.R., Nottebohm F. Monoclonal antibody reveals radial glia in adult avian brain. J. Comp. Neurol. 264:1987;159-170.
9. Alvarez-Buylla A., Kirn J.R. Birth, migration, incorporation and death of vocal control neurons in adult songbirds. J. Neurobiol. 33:1997;585-601.
10. Alvarez-Buylla A., Nottebohm F. Migration of young neurons in adult avian brain. Nature. 335:1988;353-354.
11. Alvarez-Buylla A., Temple S. Stem cells in the developing and adult nervous system. J. Neurobiol. 36:1998;105-110.
12. Armstrong R.C., Dorn H.H., Kufta C.V., Friedman E., Dubois-Dalcq M.E. Pre-oligodendrocytes from adult human CNS. J. Neurosci. 12:1992;1538-1547.
13. Barami K., Iversen K., Furneaux H., Goldman S. Early expression of the HuD protein by newly generated neurons of the adult avian forebrain. J. Neurobiol. 28:1995;82-101.
14. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50:1983;329-340.
15. Bayer S.A., Yackel J.W., Puri P.S. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science. 216:1982;890-892.
16. Belmont L.D., Mitchison T.J. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell. 84:1996;623-631.
17. Bernhardt R., Matus A. Differences in the developmental patterns of three microtubule associated proteins in the rat cerebellum. J. Neurosci. 5:1985;977-991.
18. Biffo S., Grillo M., Margolis F.L. Cellular localization of carnosine-like and anserine-like immunoreactivities in rodent and avian central nervous system. Neuroscience. 35:1990;637-651.
19. Biffo S., Marti E., Fasolo A. Carnosine, nerve growth factor receptor and tyrosine hydroxylase expression during the ontogeny of the rat olfactory system. J. Chem. Neuroanat. 5:1992;51-62.
20. Bignami A., Dahl D., Seiler M. Neurofilaments in the chick embryo during early development. Dev. Neurosci. 3:1980;151-161.
21. Bignami A., Eng L.F., Dahl D., Uyeda C.T. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43:1972;429-435.
22. Blakemore W.F. The ultrastructure of the subependymal plate in the rat. J. Anat. 104:1969;423-433.
23. Blakemore W.F., Jolly R.D. The subependymal plate and associated ependyma in the dog An ultrastructural study . J. Neurocytol. 1:1972;69-84.
24. Blaschke A.J., Weiner J.A., Chun J. Programmed cell death is a universal feature of embryonic and postnatal neuroproliferative regions throughout the central nervous system. J. Comp. Neurol. 396:1998;39-50.
25. Bonfanti L., Olive S., Poulain D.A., Theodosis D.T. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat An immunohistochemical study . Neuroscience. 49:1992;419-436.
26. Bonfanti, L.; Peretto, P.; De Marchis, S.; Fasolo, A. Carnosine-related dipeptides in the mammalian brain. Prog. Neurobiol. (in press).
27. Bonfanti L., Peretto P., Merighi A., Fasolo A. Newly generated cells from the rostral migratory stream in the accessory olfactory bulb of the adult rat. Neuroscience. 81:1997;489-502.
28. Bonfanti L., Poulain D.A., Theodosis D.T. Radial glia-like cells in the supraoptic nucleus of the adult rat. J. Neuroendocrinol. 5:1993;1-5.
29. Bonfanti L., Theodosis D.T. Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience. 62:1994;291-305.
30. Embryonic vertebrate central nervous system: Revised terminology. Anat. Rec. 166:1969;257-261.
31. Brannon-Thomas L., Gates M.A., Steindler D.A. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia. 17:1996;1-14.
32. Brennan P., Kaba H., Keverne E.B. Olfactory recognition A simple memory system . Science. 250:1990;1223-1226.
33. Brunjes P.C., Armstrong A.M. Apoptosis in the rostral migratory stream of the developing rat. Dev. Brain Res. 92:1996;219-222.
34. Bryans W.A. Mitotic activity in the brain of adult rat. Anat. Rec. 133:1959;65-71.
35. Caggiano M., Kauer S., Hunter D.D. Globose basal cells are neuronal progenitors in the olfactory epithelium A lineage analysis using a replication-incompetent retrovirus . Neuron. 13:1994;339-352.
36. Cajal, S. R. Textura del lobulo olfativo accessorio: Revista trimestral micrografica. 1:141-150; 1901.
37. Calof A.L., Mumm J.S., Rim P.C., Shou J. The neuronal stem cell of the olfactory epithelium. J. Neurobiol. 36:1998;190-205.
38. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience. 56:1993;337-344.
39. Camoletto P., Peretto P., Bonfanti L., Manceau V., Sobel A., Fasolo A. The cytosolic phosphoprotein stathmin is expressed in the olfactory system of the adult rat. NeuroReport. 8:1997;2825-2829.
40. Carden M.J., Trojanowski J.Q., Schlaepfer W.W., Lee V.M.-Y. Two stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J. Neurosci. 7:1987;3489-3504.
41. Chneiweiss A., Beretta L., Cordier J., Boutterin M.C., Glowinski J., Sobel A. Stathmin is a major phosphoprotein and cyclic AMP-dependent protein kinase substrate in mouse brain neurons but not in astrocytes in culture Regulation during ontogenesis . J. Neurochem. 53:1989;856-863.
42. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., 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. 16:1996;2649-2658.
43. Crush K.G. Carnosine and related substances in animal tissues. Comp. Biochem. Physiol. 34:1970;3-30.
44. Davis A.A., Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature. 372:1994;263-266.
45. De Marchis S., Melcangi R.C., Modena C., Cavaretta I., Peretto P., Agresti C., Fasolo A. Identification of the glial cell types containing carnosine-related peptides in the rat brain. Neurosci. Lett. 237:1997;37-40.
46. Doetsch F., Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. USA. 93:1996;14895-14900.
47. Doetsch F., García-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17:1997;5046-5061.
48. Easter S.S., Ross L.S., Frankfurter A. Initial tract formation in the mouse brain. J. Neurosci. 13:1993;285-299.
49. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nature Med. 4:1998;1313-1317.
50. Faissner A., Gotz B., Joester A., Scholze A. The tenascin gene family - versatile glycoproteins implicated in neural pattern formation and regeneration. Semin. Dev. Biol. 6:1995;139-148.
51. Farbman A.I. Olfactory neurogenesis Genetic or environmental controls? Trends Neurosci. 13:1990;362-365.
52. Farbman A.I. Developmental neurobiology of the olfactory system. Getchell T.V., Doty R.L., Bartoshuk L.M., Snow J.B. Jr. Smell and taste in health and disease. 1991;19-33 Raven Press, New York.
53. Fischer K. Subependymale Zellproliferationen und tumordisposition brachycephaler hunderassen. Acta Neuropathol. 8:1967;242-254.
54. Frederiksen K., McKay R. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8:1988;1144-1151.
55. Gadisseux J., Kadhim H.J., van den Bosh de Aguilar P., Mason C.A. Neuron migration within the radial glial fiber system of the developing murine cerebellum An electronmicroscopic autoradiographic analysis . Dev. Brain Res. 52:1990;39-56.
56. Gage F.H. Stem cells of the central nervous system. Curr. Opin. Neurobiol. 8:1998;671-676.
57. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., Ray J. Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36:1998;249-266.
58. Gage F.H., Ray J., Fisher L.J. Isolation, characterization, and use of stem cells from the CNS. Annu. Rev. Neurosci. 18:1995;159-192.
59. Garcia-Verdugo J.M., Doetsch F., Wichterle H., Lim D.A., Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone In search of the stem cells . J. Neurobiol. 36:1998;234-248.
60. Gates M.A., Thomas L.B., Howard E.M., Laywell E.D., Sajin B., Faissner A., Gotz B., Silver J., Steindler D.A. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 361:1995;249-266.
61. Globus J.H., Kuhlenbeck H. The subependymal cell plate (matrix) and its relationship to brain tumors of the ependymal type. J. Neuropathol. 3:1944;1-35.
62. Goldman S.A. Comparative strategies of subependymal neurogenesis in the adult forebrain. Gage F.H., Christen Y. Isolation, characterization and utilization of CNS stem cells. 1997;43-65 Springer-Verlag, Berlin.
63. Goldman S.A., Luskin M.B. Strategies utilized by migrating neurons of the postnatal vertebrate forebrain. Trends Neurosci. 21:1998;107-114.
64. Gould E., Tanapat P., McEwen B.S., 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. 95:1998;3168-3171.
65. Gray H. Gray's anatomy. 37th ed. 1989;Longman Group UK Ltd, London.
66. Graziadei P.P.C., Monti-Graziadei G.A. Continuous nerve cell renewal in the olfactory system. Jacobson M. Handbook of sensory physiology. 1978;55-83 Springer-Verlag, Berlin.
67. Graziadei P.P.C., Monti Graziadei G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals, I Morphological aspects of differentiation and structural organization of the olfactory neurons . J. Neurocytol. 8:1979;1-18.
68. Gregory W.A., Edmondson J.C., Hatten M.E., Mason C.A. Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J. Neurosci. 8:1988;1728-1738.
69. Gritti A., Parati E.A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D.J., Roisen F., Nickel D.D., Vescovi A.L. Multipotential stem cells from the adult mouse brain proliferate and self renew in response to basic fibroblast growth factor. J. Neurosci. 16:1996;1091-1100.
70. Hauke C., Ackermann I., Korr H. Cell proliferation in the subependymal layer of the adult mouse in vivo and in vitro. Cell Prolif. 28:1995;595-607.
71. Hinds J.W. Autoradiographic study of histogenesis in the mouse olfactory bulb, I Time of origin of neurons and neuroglia . J. Comp. Neurol. 134:1968;287-304.
72. Hinds J.W. Autoradiographic study of histogenesis in the mouse olfactory bulb, II Cell proliferation and migration . J. Comp. Neurol. 134:1968;305-322.
73. Holcomb J.D., Mumm J.S., Calof A.L. Apoptosis in the neuronal lineage of the mouse olfactory epithelium Regulation in vivo and in vitro . Dev. Biol. 172:1995;307-323.
74. Hu H., Tomasiewicz H., Magnuson T., Rutishauser U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron. 16:1996;735-743.
75. Ikuta F. Morphology of migrating glial cells in normal development, neoplasia and other disorders. Zimmerman H.M. Progress in neuropathology. 1979;337-405 Raven Press, New York.
76. Jacobson M. Developmental neurobiology. 1991;Plenum Press, New York.
77. Jankovski A., Sotelo C. Subventricular zone-olfactory bulb migratory pathway in the adult mouse Cellular composition and specificity as determined by heterochronic and heterotopic transplantation . J. Comp. Neurol. 371:1996;376-396.
78. Johansson C.B., Momma S., Clarke D.L., Risling M., Lendahl U., Frisén J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 96:1999;25-34.
79. Kaba H., Hayashi Y., Higuchi T., Nakanishi S. Induction of an olfactory memory by the activation of a metabotropic glutamate receptor. Science. 265:1994;262-264.
80. Kaplan M.S. Proliferation of ependymal cells in the adult primate CNS Differential uptake of DNA labeled precursors . J. Hirnforsch. 24:1983;23-33.
81. Kaplan M.S., Bell D.H. Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J. Neurosci. 4:1984;1429-1441.
82. Kaplan M.S., Hinds J.W. Neurogenesis in the adult rat Electron microscopic analysis of light radioautographs . Science. 197:1977;1092-1094.
83. Kaplan M.S., McNelly N.A., Hinds J.W. Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J. Comp. Neurol. 239:1985;117-125.
84. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18:1998;3206-3212.
85. Kilpatrick T.J., Bartlett P.F. Cloning and growth of multipotential neural precursors Requirements for proliferation and differentiation . Neuron. 10:1993;255-265.
86. Kirschenbaum B., Goldman S.A. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. USA. 92:1995;210-214.
87. Kirschenbaum B., Nedergaard M., Preuss A., Barami K., Fraser R.A.R., Goldman S.A. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb. Cortex. 6:1994;576-589.
88. Kishi K. Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J. Comp. Neurol. 258:1987;112-124.
89. Kishi K., Peng J.Y., Kakuta S., Murakami K., Kuroda M., Yokota S., Hayakawa S., Kuge T., Asayama T. Migration of bipolar subependymal cells, precursors of the granule cells of the rat olfactory bulb, with reference to the arrangement of the radial glial fibers. Arch. Histol. Cytol. 53:1990;219-226.
90. Kohen R., Yamamoto Y., Cundy K.C., Ames B.N. Antioxidant activity of carnosine, homocarnosine and anserine present in muscle and brain. Proc. Natl. Acad. Sci. USA. 85:1988;3175-3179.
91. Koppel J., Boutterin M.C., Doye V., Peyro-Saint Paul H., Sobel A. Developmental tissue expression and phylogenetic conservation of stathmin, a phosphoprotein associated with cell regulation. J. Biol. Chem. 265:1990;3703-3707.
92. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat Age-related decrease of neuronal progenitor proliferation . J. Neurosci. 16:1996;2027-2033.
93. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects of neural progenitors in the adult rat brain. J. Neurosci. 17:1997;5820-5829.
94. LaMantia A., Pomeroy S.L., Purves D. Vital imaging of glomeruli in the mouse olfactory bulb. J. Neurosci. 12:1992;976-988.
95. Larriva-Sahd J., Matsumoto A. The vomeronasal system and its connections with sexually dimorphic neural structures. Zool. Sci. 11:1994;495-506.
96. Latov N., Nilaver G., Zimmerman E.A., Johnson W.G., Silverman A-J, Defendini R., Cote L. Fibrillary astrocytes proliferate in response to brain injury. Dev. Biol. 72:1979;381-384.
97. Lee M.K., Rebhun L.I., Frankfurter A. Posttranslational modification of class III β-tubulin. Proc. Natl. Acad. Sci. USA. 87:1990;7195-7199.
98. Lee M.K., Tuttle J.B., Rebhun L.I., Cleveland D.W., Frankfurter A. The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskel. 17:1990;118-132.
99. Lendahl U., Zimmerman L.B., McKay R.D.G. CNS stem cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
100. Levison S.W., Chuang C., Abramson B.J., Goldman J.E. The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development. 119:1993;611-622.
101. Levison S.W., Goldman J.E. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron. 10:1993;201-212.
102. Lewis P.D. Mitotic activity in the primate sub-ependymal layer and the genesis of gliomas. Nature. 217:1968;974-975.
103. Loeffler M., Potten C.S. Stem cells and cellular pedigrees - a conceptual introduction. Potten C.S. Stem cells. 1997;1-27 Academic Press, London.
104. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 264:1994;1145-1148.
105. Lois C., Garcia-Verdugo J., Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 271:1996;978-981.
106. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
107. Luskin M.B. Neuronal cell lineage in the vertebrate central nervous system. FASEB J. 8:1994;722-730.
108. Luskin M.B., Boone M.S. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses. 19:1994;695-714.
109. Luskin M.B., McDermott K. Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia. 11:1994;211-226.
110. Luskin M.B., Zigova T., Betarbet R., Soteres B.J. Characterization of neuronal progenitor cells of the neonatal forebrain. Gage F.H., Christen Y. Isolation, characterization and utilization of CNS stem cells. 1997;67-86 Springer-Verlag, Berlin.
111. Marusich M., Weston J. Identification of early neurogenic cells in the neural crest lineage. Dev. Biol. 149:1992;295-306.
112. Mathews M.B., Bernstein R.M., Franza B.R. Jr, Garrels J.I. Identity of the proliferating cell nuclear antigen and cyclin. Nature. 309:1984;374-376.
113. Matus A., Mughal S. Immunohistochemical localisation of S-100 protein in brain. Nature. 258:1975;746-748.
114. McConnell S.K. The generation of neuronal diversity in the central nervous system. Annu. Rev. Neurosci. 14:1991;269-300.
115. McDermott K.W.G., Lantos P.L. Cell proliferation in the subependymal layer of the postnatal marmoset, Callithrix jacchus. Dev. Brain Res. 57:1990;269-277.
116. McDermott K.W., Luskin M.B. The use of retroviral vectors in the study of cell lineage and migration during the development of the mammalian central nervous system. Kaplitt M.G., Loewy A.D. Viral vectors. 1995;411-433 Academic Press, San Diego, CA.
117. McKay R. Stem cells in the central nervous system. Science. 276:1997;66-71.
118. Menezes J.R.L., Luskin M.B. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 14:1994;5399-5416.
119. Menezes J.R.L., Smith C.M., Nelson K.C., Luskin M.B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6:1995;496-508.
120. Miller M.W., Nowakowski R.S. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of the cells in the central nervous system. Brain Res. 457:1988;44-52.
121. Miragall F., Kadmon G., Faissner A., Antonicek H., Schachner M. Retention of J1/tenascin and the polysialylated form of the neural cell adhesion molecule (N-CAM) in the adult olfactory bulb. J. Neurocytol. 19:1990;899-914.
122. Misson J.P., Edwards M.A., Yamamoto M., Caviness V.S. Jr. Identification of radial glial cells within the developing murine central nervous system Studies based upon a new immunohistochemical marker . Dev. Brain Res. 44:1988;95-108.
123. Moran D.T., Jafek B.W., Carter Rowley J. III. The vomeronasal (Jacobson's) organ in man: Ultrastructure and frequency of occurrence. J. Steroid Biochem. Molec. Biol. 39:1991;545-552.
124. Morrison S.J., Shah N.M., Anderson D.J. Regulatory mechanisms in stem cell biology. Cell. 88:1997;287-298.
125. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., van der Koy D. Neural stem cells in the adult mammalian forebrain A relatively quiescent subpopulation of subependymal cells . Neuron. 13:1994;1071-1082.
126. Morshead C.M., van der Kooy D. Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J. Neurosci. 12:1992;249-256.
127. Najbauer J., Leon M. Olfactory experience modulates apoptosis in the developing olfactory bulb. Brain Res. 674:1995;245-251.
128. Ono K., Tomasiewicz H., Magnuson T., Rutishauser U. N-Cam mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron. 13:1994;595-609.
129. O'Rourke N. Neuronal chain gangs Homotypic contacts support migration into the olfactory bulb . Neuron. 16:1996;1061-1064.
130. O'Rourke N.A., Dailey M.E., Smith S.J., McConnell S.K. Diverse migratory pathways in the developing cerebral cortex. Science. 258:1992;299-302.
131. Palmer T.D., Ray J., Gage F.H. FGF-2 responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6:1995;474-486.
132. Peretto P., Bonfanti L., Merighi A., Fasolo A. Carnosine-like immunoreactivity in astrocytes of the glial tubes and in newly generated cells within the tangential part of the rostral migratory stream of rodents. Neuroscience. 85:1998;527-542.
133. Peretto P., Merighi A., Fasolo A., Bonfanti L. Glial tubes in the rostral migratory stream of the adult rat. Brain Res. Bull. 42:1997;9-21.
134. Peschanski M., Doye V., Hirsch E., Marty L., Dusart I., Manceau V., Sobel A. Stathmin Cellular localization of a major phosphoprotein in the adult rat CNS, with a note on human forebrain . J. Comp. Neurol. 337:1993;655-668.
135. Peters W., Peters A., Palay S.L., Webster H.D. The fine structure of the nervous system. 1976;264-270 WB Saunders Company, Philadelphia.
136. Pinching A.J., Powell T.P.S. The neuron types of the glomerular layer of the olfactory bulb. J. Cell Sci. 9:1971;305-345.
137. Pixley S.K.R., De Vellis J. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Dev. Brain Res. 15:1984;201-209.
138. Pomeroy S.L., LaMantia A.S., Purves D. Postnatal construction of neural circuitry in the mouse olfactory bulb. J. Neurosci. 10:1990;1952-1966.
139. Potten C.S., Loeffler M. Stem cells Attributes, cycles, spirals, pitfalls and uncertainties - lesson for and from the crypt . Development. 110:1990;1001-1020.
140. Price J.P. The morphology of granule cells of the olfactory bulb. J. Cell Sci. 7:1970;91-123.
141. Privat A., Leblond C.P. The subependymal layer and neighboring region in the brain of the young rat. J. Comp. Neurol. 146:1972;277-302.
142. Purves D., Lichtman J.W. Principles of neural development. 1985;Sinauer, Sunderland, MA.
143. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33:1971;471-476.
144. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex A Golgi and electronmicroscopic study in Macacus rhesus . J. Comp. Neurol. 141:1971;283-312.
145. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145:1972;61-83.
146. Rakic P. Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. USA. 92:1996;11323-11327.
147. Ramon-Cueto A., Valverde F. Olfactory bulb ensheathing glia A unique cell type with axonal growth-promoting properties . Glia. 14:1995;163-173.
148. Ray J., Palmer T.D., Suhonen J., Takahashi J., Gage F.H. Neurogenesis in the adult brain Lesson learned from the studies of progenitor cells from the embryonic and adult central nervous system . Gage F.H., Christen Y. Isolation, characterization and utilization of CNS stem cells. 1997;128-148 Springer-Verlag, Berlin.
149. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1992;1707-1710.
150. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175:1996;1-13.
151. Richards K.J., Kilpatrick T.J., Bartlett P.F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. USA. 9:1992;8591-8595.
152. Rougon G. Structure, metabolism and cell biology of polysialic acids. Eur. J. Cell Biol. 61:1993;197-207.
153. Rousselot P., Lois C., Alvarez-Buylla A. Embryonic (psa) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351:1995;51-61.
154. Saga Y., Yagi T., Ikawa Y., Sakakura T., Aizawa S. Mice develop normally without tenascin. Genes Dev. 6:1992;1821-1831.
155. Schlessinger A.R., Cowan W.M., Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 159:1975;149-176.
156. Seki T., Arai Y. Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol. 184:1991;395-401.
157. Shaw G., Osborn M., Weber K. An immunofluorescence microscopical study of the neurofilament triplet proteins, vimentin and glial fibrillary acidic protein within the adult rat brain. Eur. J. Cell Biol. 26:1981;68-82.
158. Smart I. The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J. Comp. Neurol. 116:1961;325-338.
159. 3. J. Comp. Neurol. 116:1961;349-367.
160. Sobel A. Stathmin A relay phosphoprotein for multiple signal transduction? Trends Biochem. Sci. 16:1991;301-305.
161. Stanfield B.B., Trice J.E. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res. 72:1988;399-406.
162. Steindler D.A. Glial boundaries in the developing nervous system. Annu. Rev. Neurosci. 16:1993;445-470.
163. Sturrock R.R. Quantitative changes in neuroglia in the white matter of the mouse brain following hypoxic stress. J. Anat. 121:1976;7-13.
164. Sturrock R.R. Electron microscopic evidence for mitotic division of oligodendrocytes. J. Anat. 131:1981;577-582.
165. Switzer R.C., De Olmos J.S., Heimer L. Olfactory system. Paxinos G. The rat nervous system. vol 1:1985;1-36 Academic Press, Sydney.
166. Szabo A., Dalmau J., Manley G., Rosenfeld M., Wong E., Henson J., Posner J.B., Furneaux H.M. HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to elav and sex-lethal. Cell. 67:1991;325-333.
167. Takahashi T., Nowakowski R.S., Caviness V.S. Jr. Cell cycle parameters and patterns of nuclear movements in the neocortical proliferative zone of the fetal mouse. J. Neurosci. 13:1993;820-833.
168. Takahashi,T.; Nowakowski, R. S.; Caviness, V. S. Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15:6046-6057; 1995.
169. Takahashi,T.; Nowakowski, R. S.; Caviness, V. S. Jr. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J. Neurosci. 15:6058-6068; 1995.
170. Theodosis D.T., Poulain D.A. Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus. Neuroscience. 57:1993;501-535.
171. Tohyama T., Lee V.M.-Y., Rorke L.B., Trojanowski J.Q. Molecular milestones that signal axonal maturation and the commitment of human spinal cord precursor cells to the neuronal or glial phenotype in development. J. Comp. Neurol. 310:1991;285-299.
172. Tomasiewicz H., Ono K., Yee D., Thompson C., Goridis C., Rutishauser U., Magnuson T. Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron. 11:1993;1163-1174.
173. Tropepe V., Craig C.G., Morshead C.M., van der Kooy D. Transforming growth factor-a null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 17:1997;7850-7859.
174. Vescovi A.L., Reynolds B.A., Fraser D.D., Weiss S. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron. 11:1993;951-966.
175. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16:1996;7599-7609.
176. Weiss S., Reynolds B.A., Vescovi A.L., Morshead C., Craig C.G., van der Kooy D. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci. 19:1996;387-393.
177. Weiss S., van der Kooy D. CNS stem cells: Where's the biology (a.k.a. beef)? J. Neurobiol. 36:1998;307-314.
178. Wichterle H., Garcia-Verdugo J.M., Alvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron. 18:1997;779-791.
179. Wolff J.R., Missler M. Synaptic reorganization in developing and adult nervous systems. Ann. Anat. 174:1992;393-403.
180. Yang P., Yin X., Rutishauser U. Intercellular space is affected by the polysialic acid content of N-CAM. J. Cell Biol. 116:1992;1487-1496.
181. Young G.M., Levison S.W. Persistence of multipotential progenitors in the juvenile rat subventricular zone. Dev. Neurosci. 18:1996;255-265.
182. Zerlin M., Levison S.W., Goldman J.E. Early patterns of migration, morphogenesis, and intermediate filaments expression of subventricular zone cells in the postnatal rat forebrain. J. Neurosci. 15:1995;7238-7249.
183. Zigova T., Betarbet R., Soteres B.J., Brock S., Bakay R.A.E., Luskin M.B. A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted tenencephalic ventricular zone cells. Dev. Biol. 173:1996;459-474.
184. Zigova T., Pencea V., Wiegand S.J., Luskin M.B. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 11:1998;234-245.