Prenatal development of the rodent rostral migratory stream

Journal of Comparative Neurology

Volumn 463, Issue 4, 2003, Pages 402-418

  Pencea, Viorica ^a   Luskin, Marla B ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell proliferation; Forebrain development; Prenatal neurogenesis; Subventricular zone; Telencephalon; Ventricular zone

Indexed keywords

BROXURIDINE;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CELL PROLIFERATION; CELL SPECIFICITY; CELL TYPE; CYTOARCHITECTURE; EMBRYO; EMBRYO DEVELOPMENT; FOREBRAIN; MITOSIS RATE; NEWBORN; NONHUMAN; OLFACTORY BULB; PHENOTYPE; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; RODENT; ROSTRAL MIGRATORY STREAM;

ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL DIVISION; CELL MOVEMENT; CEREBRAL VENTRICLES; IMMUNOHISTOCHEMISTRY; NEURAL CELL ADHESION MOLECULE L1; NEURONS; OLFACTORY BULB; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; SIALIC ACIDS; STEM CELLS;

EID: 0038781298     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10746     Document Type: Article

References (91)

1. Allen E. 1912. The cessation of mitosis in the central nervous system of the albino rat. J Comp Neurol 19:547-568.
2. 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 137:433-457.
3. Altman J, Bayer SA. 1990. Horizontal compartmentation in the germinal matrices and intermediate zone of the embryonic rat cerebral cortex. Exp Neurol 107:36-47.
4. Altman J, Das GD. 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 126:337-389.
5. Alves JA, Barone P, Engelender S, Froes M, Menezes JRL. 2002. Initial stages of radial glia astrocytic transformation in the early postnatal anterior subventricular zone. J Neurobiol 52:51-65.
6. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
7. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329-340.
8. Bayer SA. 1985. Neuron production in the hippocampus and olfactory bulb of the adult rat brain: addition or replacement? Ann N Y Acad Sci 457:163-172.
9. Bayer SA, Altman J, Russo RJ, Zhang X. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83-144.
10. Bernhardt R, Huber G, Matus A. 1985. Differences in the developmental patterns of three microtubule-associated proteins in the rat cerebellum. J Neurosci 5:977-991.
11. Betarbet R, Zigova T, Bakay RA, Luskin MB. 1996. Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int J Dev Neurosci 14:921-930.
12. Bhide PG. 1996. Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 374:506-522.
13. Bignami A, Eng LF, Dahl D, Uyeda CT. 1972. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429-435.
14. Bonfanti L, Olive S, Poulain DA, Theodosis DT. 1992. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49:419-436.
15. Brock SC, Bonsall J, Luskin MB. 1998. The neuronal progenitor cells of the forebrain subventricular zone: intrinsic properties in vitro and following transplantation. Methods: A Companion to Methods in Enzymology 16:268-281.
16. Byrd CA, Burd GD. 1993. The quantitative relationship between olfactory axons and mitral/tufted cells in developing Xenopus with partially deafferented olfactory bulbs. J Neurobiol 24:1229-1242.
17. 3H]thymidine autoradiography. Brain Res 256:293-302.
18. Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H. 2000. Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20:1446-1457.
19. Coskun V, Luskin MB. 2001. The expression pattern of the cell cycle inhibitor p19(INK4d) by progenitor cells of the rat embryonic telencephalon and neonatal anterior subventricular zone. J Neurosci 21:3092-3103.
20. Covault J, Sanes JR. 1986. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol 102:716-730.
21. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, et al. 1994. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
22. 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.
23. Doetsch F, Garcia-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.
24. Edmondson JC, Hatten ME. 1987. Glial-guided granule neuron migration in vitro: a high-resolution time-lapse video microscopic study. J Neurosci 7:1928-1934.
25. Farbman AI. 1992. Development of the olfactory bulb. In: Barlow PW, Bray D, Green PB, Slack JMW, editors. Cell Biology of Olfaction. New York: Cambridge University Press. p 181-183.
26. Frederiksen K, McKay RD. 1988. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144-1151.
27. Goldman JE. 1995. Lineage, migration, and fate determination of postnatal subventricular zone cells in the mammalian CNS. J Neurooncol 24:61-64.
28. Gong Q, Shipley MT. 1995. Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14:91-101.
29. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15-30.
30. Hatten ME. 1990. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13:179-184.
31. Hinds JW. 1968. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
32. Hockfield S, McKay RD. 1985. Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
33. Hogan BL, Horsburgh G, Cohen J, Hetherington CM, Fisher G, Lyon MF. 1986. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation ofboth lens and nasal placodes in the mouse. J Embryol Exp Morphol 97:95-110.
34. Hu H. 2000. Polysialic acid regulates chain formation by migrating olfactory interneuron precursors. J Neurosci Res 61:480-492.
35. Hu H, Rutishauser U. 1996. A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16:933-940.
36. Jankovski A, Garcia C, Soriano E, Sotelo C. 1998. Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 10:3853-3868.
37. Johnson GV, Jope RS. 1992. The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res 33:505-512.
38. Kaufman DL, McGinnis JF, Krieger NR, Tobin AJ. 1986. Brain glutamate decarboxylase cloned in lambda gt-11: fusion protein produces gamma-aminobutyric acid. Science 232:1138-1140.
39. Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A. 1999. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci 19:2171-2180.
40. Kishi K, Peng JY, Kakuta S, Murakami K, Kuroda M, Yokota S, Hayakawa S, Kuge T, Asayama T. 1990. 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 53:219-226.
41. Kornack DR, Rakic P. 2001. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752-4757.
42. LaMantia AS, Colbert MC, Linney E. 1993. Retinoic acid induction and regional differentiation prefigure olfactory pathway formation in the mammalian forebrain. Neuron 10:1035-1048.
43. Law AK, Pencea V, Buck CR, Luskin MB. 1999. Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes. Dev Biol 216:622-634.
44. Lee MK, Rebhun LI, Frankfurter A. 1990. Posttranslational modification of class III beta-tubulin. Proc Natl Acad Sci USA 87:7195-7199.
45. Lendahl U, McKay RD. 1990. The use of cell lines in neurobiology. Trends Neurosci 13:132-137.
46. LeVine SM, Goldman JE. 1988a. Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci 8:3992-4006.
47. LeVine SM, Goldman JE. 1988b. Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. J Comp Neurol 277:441-455.
48. Levison SW, Chuang C, Abramson BJ, Goldman JE. 1993. The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119:611-622.
49. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
50. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. 1996. Chain migration of neuronal precursors. Science 271:978-981.
51. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
52. Luskin MB. 1994. Neuronal cell lineage in the vertebrate central nervous system. FASEB J 8:722-730.
53. Luskin MB, McDermott K. 1994. Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 11:211-226.
54. Luskin MB, Shatz CJ. 1985. Neurogenesis of the cat's primary visual cortex. J Comp Neurol 242:611-631.
55. Luskin MB, Zigova T, Soteres BJ, Stewart RR. 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.
56. Luskin MB, Coskun V. 2002. The progenitor cells of the embryonic telencephalon and the neonatal anterior subventricular zone differentially regulate their cell cycle. Chem Senses 27:577-580.
57. McConnell SK. 1988. Development and decision-making in the mammalian cerebral cortex. Brain Res 472:1-23.
58. McConnell SK. 1989. The determination of neuronal fate in the cerebral cortex. Trends Neurosci 12:342-349.
59. Menezes JR, Smith CM, Nelson KC, Luskin MB. 1995. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol Cell Neurosci 6:496-508.
60. Menezes JR, Dias F, Garson AV, Lent R. 1998. Restricted distribution of S-phase cells in the anterior subventricular zone of the postnatal mouse forebrain. Anat Embryol 198:205-211.
61. Meyers EN, Lewandoski M, Martin GR. 1998. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18:136-141.
62. Nowakowski RS, Hayes NL. 1999. CNS development: an overview. Dev Psychopathol 11:395-417.
63. O'Rourke NA, Dailey ME, Smith SJ, McConnell SK. 1992. Diverse migratory pathways in the developing cerebral cortex. Science 258:299-302.
64. Pencea V, Smith CM, Luskin MB. 1998. Characterization of the rostral migratory stream during mammalian forebrain development. Soc Neurosci Abstr 24:787.
65. Pencea V, Bingaman KD, Freedman LJ, Luskin MB. 2001. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1-16.
66. Peretto P, Merighi A, Fasolo A, Bonfanti L. 1997. Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42:9-21.
67. Peretto P, Merighi A, Fasolo A, Bonfanti L. 1999. The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull 49:221-243.
68. Porteus MH, Bulfone A, Liu JK, Puelles L, Lo LC, Rubenstein JL. 1994. DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J Neurosci 14:6370-6383.
69. Privat A. 1975. Postnatal gliogenesis in the mammalian brain. Int Rev Cytol 40:281-323.
70. Raedler E, Raedler A. 1978. Autoradiographic study of early neurogenesis in rat neocortex. Anat Embryol 154:267-284.
71. Rakic P. 1971. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471-476.
72. Rakic P. 1974. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
73. Rakic P. 1990. Principles of neural cell migration. Experientia 46:882-891.
74. Rosselli-Austin L, Altman J. 1979. The postnatal development of the main olfactory bulb of the rat. J Dev Physiol 1:295-313.
75. Rousselot P, Lois C, Alvarez-Buylla A. 1995. 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.
76. Rutishauser U, Landmesser L. 1996. Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci 19:422-427.
77. Sanes JR, Schachner M, Covault J. 1986. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol 102:420-431.
78. Schwob JE, Price JL. 1984. The development of lamination of afferent fibers to the olfactory cortex in rats, with additional observations in the adult. J Comp Neurol 223:203-222.
79. Sheth AN, Bhide PG. 1997. Concurrent cellular output from two proliferative populations in the early embryonic mouse corpus striatum. J Comp Neurol 383:220-230.
80. Skoff RP, Knapp PE. 1991. Division of astroblasts and oligodendroblasts in postnatal rodent brain: evidence for separate astrocyte and oligodendrocyte lineages. Glia 4:165-174.
81. Smart IH. 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.
82. Stenman J, Toresson H, Campbell K. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174.
83. Stewart RR, Hoge GJ, Zigova T, Luskin MB. 2002. Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J Neurobiol 50:305-322.
84. Stout RP, Graziadei PP. 1980. Influence of the olfactory placode on the development of the brain in Xenopus laevis (Daudin). I. Axonal growth and connections of the transplanted olfactory placode. Neuroscience 5:2175-2186.
85. Stuhmer T, Puelles L, Ekker M, Rubenstein JL. 2002. Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75-85.
86. Sturrock RR, Smart IH. 1980. A morphological study of the mouse subependymal layer from embryonic life to old age. J Anat 130:391-415.
87. Takahashi T, Nowakowski RS, Caviness VS Jr. 1994. Mode of cell proliferation in the developing mouse neocortex. Proc Natl Acad Sci USA 91:375-379.
88. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T. 1993. Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174.
89. Voigt T. 1989. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74-88.
90. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. 2001. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
91. Zigova T, Betarbet R, Soteres BJ, Brock S, Bakay RA, Luskin MB. 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.