Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes

Developmental Biology

Volumn 216, Issue 2, 1999, Pages 622-634

  Law, Alick K T ^a   Pencea, Viorica ^a   Buck, Charles R ^a   Luskin, Marla B ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Development; Forebrain; Neurogenesis; Olfactory bulb; Progenitor cell

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN VENTRICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; FOREBRAIN; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; MACROGLIA; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ANIMALIA;

EID: 0033572615     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9498     Document Type: Article

References (60)

1. Akimoto J., Itoh H., Miwa T., Ikeda K. Immunohistochemical study of glutamine synthetase expression in early glial development. Dev. Brain Res. 72:1993;9-14.
2. 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;433-457.
3. Bayer S. A. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50:1983;329-340.
4. Bond J. F., Farmer S. R. Regulation of tubulin and actin mRNA production in rat brain: Expression of a new beta-tubulin mRNA with development. Mol. Cell. Biol. 3:1983;1333-1342.
5. Bond J. F., Robinson G. S., Farmer S. R. Differential expression of two neural cell-specific beta-tubulin mRNAs during rat brain development. Mol. Cell. Biol. 4:1984;1313-1319.
6. Carden M. J., Trojanowski J. Q., Schlaepfer W. W., Lee V. M. Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J. Neurosci. 7:1987;3489-3504.
7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
8. Cremer H., Lange R., Christoph A., Plomann M., Vopper G., Roes J., Brown R., Baldwin S., Kraemer P., Scheff S., Barthels D., Rajewsky K., Wille W. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 367:1994;455-459.
9. Doetsch F., Caille I., Lim D. A., Garcia-Verdugo J. M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:1999;703-716.
10. Easter S. S. Jr., Ross L. S., Frankfurter A. Initial tract formation in the mouse brain. J. Neurosci. 13:1993;285-299.
11. Ellison J. A., Scully S. A., de Vellis J. Evidence for neuronal regulation of oligodendrocyte development: Cellular localization of platelet-derived growth factor alpha receptor and A-chain mRNA during cerebral cortex development in the rat. J. Neurosci. Res. 45:1996;28-39.
12. Freeman R. S., Estus S., Johnson E. M. Jr. Analysis of cell cycle-related gene expression in postmitotic neurons: Selective induction of Cyclin D1 during programmed cell death. Neuron. 12:1994;343-355.
13. Gates M. A., Thomas L. B., Howard E. M., Laywell E. D., Sajin B., Faissner A., Götz 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.
14. Ginzburg I., Teichman A., Griffin W. S., Littauer U. Z. Differential expression of alpha-tubulin mRNA in rat cerebellum as revealed by in situ hybridization. FEBS Lett. 194:1986;161-164.
15. Halliday A. L., Cepko C. L. Generation and migration of cells in the developing striatum. Neuron. 9:1992;15-26.
16. Hatten M. E. Riding the glial monorail: A common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 13:1990;179-184.
17. Jiang Y. Q., Oblinger M. M. Differential regulation of beta III and other tubulin genes during peripheral and central neuron development. J. Cell Sci. 103:1992;643-651.
18. 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.
19. 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.
20. Law A. K. T., Varadarajan U., Coskun V., Luskin M. B., Buck C. R. Gene expression in the postnatal rat anterior subventricular zone, a neuronal progenitor population. Soc. Neurosci. Abstr. 24:1998;1277.
21. Lendahl U., Zimmerman L. B., McKay R. D. CNS stem cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
22. LeVine S. M., Goldman J. E. Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J. Neurosci. 8:1988;3992-4006.
23. 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.
24. 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.
25. Levison S. W., Goldman J. E. Multipotential and lineage restricted precursors coexist in the mammalian perinatal subventricular zone. J. Neurosci. Res. 48:1997;83-94.
26. Lewis S. A., Balcarek J. M., Krek V., Shelanski M., Cowan N. J. Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: Structural conservation of intermediate filaments. Proc. Natl. Acad. Sci. USA. 81:1984;2743-2746.
27. Lim D. A., Alvarez-Buylla A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl. Acad. Sci. USA. 96:1999;7526-7531.
28. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 264:1994;1145-1148.
29. Lois C., García-Verdugo J. M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 271:1996;978-981.
30. Luskin M. B. Restricted proliferation and migration of postnatallly generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
31. Luskin M. B., McDermott K. Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia. 11:1994;211-226.
32. Luskin M. B., Parnavelas J. G., Barfield J. A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: An ultrastructural analysis of clonally related cells. J. Neurosci. 13:1993;1730-1750.
33. Luskin M. B., Zigova T., Soteres B. J., Stewart R. R. 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. 8:1997;351-366.
34. Ma Q., Sommer L., Cserjesi P., Anderson D. J. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J. Neurosci. 17:1997;3644-3652.
35. McKinney M., Robbins M. Chronic atropine administration up-regulates rat cortical muscarinic m1 receptor mRNA molecules: Assessment with the RT/PCR. Mol. Brain Res. 12:1992;39-45.
36. Mearow K. M., Mill J. F., Vitkovic L. The ontogeny and localization of glutamine synthetase gene expression in rat brain. Mol. Brain Res. 6:1989;223-232.
37. Memberg S. P., Hall A. K. Dividing neuron precursors express neuron-specific tubulin. J. Neurobiol. 27:1995;26-43.
38. Menezes J. R., 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.
39. Miller F. D., Naus C. C., Durand M., Bloom F. E., Milner R. J. Isotypes of alpha-tubulin are differentially regulated during neuronal maturation. J. Cell. Biol. 105:1987a;3065-3073.
40. Miller F. D., Naus C. C., Higgins G. A., Bloom F. E., Milner R. J. Developmentally regulated rat brain mRNAs: Molecular and anatomical characterization. J. Neurosci. 7:1987b;2433-2444.
41. Mullen R. J., Buck C. R., Smith A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 116:1992;201-211.
42. Okano H. J., Darnell R. B. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17:1997;3024-3037.
43. Oumesmar B. N., Vignais L., Baron-Van Evercooren A. Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS. J. Neurosci. 17:1997;125-139.
44. 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.
45. Privat A. Postnatal gliogenesis in the mammalian brain. Int. Rev. Cytol. 40:1975;281-323.
46. Rakic P. Principles of neural cell migration. Experientia. 46:1990;882-891.
47. Redmond L., Hockfield S., Morabito M. A. The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb. J. Neurosci. 16:1996;2972-2982.
48. Schaeren-Wiemers N., Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: In situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry. 100:1993;431-440.
49. Schmechel D. E., Brightman M. W., Marangos P. J. Neurons switch from nonneuronal enolase to neuron-specific enolase during differentiation. Brain Res. 190:1980;195-214.
50. Schwob J. R., Farber N. B., Gottlieb D. I. Neurons of the olfactory epithelium in adult rats contain vimentin. J. Neurosci. 6:1986;208-217.
51. Smith C. M., Luskin M. B. Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev. Dyn. 213:1998;220-227.
52. Thomas L. B., 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.
53. 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.
54. Vaysse P. J., Goldman J. E. A clonal analysis of glial lineages in neonatal forebrain development in vitro. Neuron. 5:1990;227-235.
55. Wichterle H., Garcia-Verdugo J. M., Alvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron. 18:1997;779-791.
56. Wu W., Wong K., Chen J., Jiang Z., Dupuis S., Wu J. Y., Rao Y. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature. 400:1999;331-336.
57. Zerlin M., Levison S. W., Goldman J. E. Early patterns of migration, morphogenesis, and intermediate filament expression of subventricular zone cells in the postnatal rat forebrain. J. Neurosci. 15:1995;7238-7249.
58. Zhang M. Z., McKanna J. A. Gliogenesis in postnatal rat optic nerve: LC1 + microglia and S100-beta + astrocytes. Dev. Brain Res. 101:1997;27-36.
59. Zigova T., Betarbet R., Soteres B. J., Brock S., Bakay R. A., Luskin M. B. 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. 173:1996;459-474.
60. Zigova T., Pencea V., Betarbet R., Wiegand S. J., Alexander C., Bakay R. A., Luskin M. B. Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant. 7:1998;137-156.