Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb

Journal of Neuroscience

Volumn 19, Issue 6, 1999, Pages 2171-2180

  Kirschenbaum, Barry ^a   Doetsch, Fiona ^a   Lois, Carlos ^b   Alvarez Buylla, Arturo ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Adult; Bulbectomy; Cell death; Neuronal precursors; Subependymal layer; Subventricular zone

Indexed keywords

BROXURIDINE; DNA NUCLEOTIDYLEXOTRANSFERASE;

ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DENSITY; CELL DIFFERENTIATION; CELL DIVISION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; LATERAL BRAIN VENTRICLE; MOUSE; NERVE CELL; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY BULBECTOMY; PRIORITY JOURNAL; TELENCEPHALON;

EID: 0033559771     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-06-02171.1999     Document Type: Article

References (57)

1. Ahmed S, Reynolds BA, Weiss S (1995) BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci 15:5765-5778.
2. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forehrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433-458.
3. Alvarez-Buylla A (1997) Mechanism of migration of olfactory bulh interncurons. Semin Cell Dev Biol 8:207-213.
4. Alvarcz-Buylla A, Vicario DS (1988) Simple microcomputer system for mapping tissue sections with the light microscope. J Neurosci Methods 25:165-173.
5. Alvarez-Buylla A. Buskirk DR, Nottehohm F (1987) Monoclonal antibody reveals radial glia in adult avian brain. J Comp Neurol 264:l59-170.
6. Alvarez-Buylla A, Theelen M, Nottebohm F (1988) Birth of projection neurons in the higher vocal center of the canary forcbrain before, during, and after song learning. Proc Natl Acad Sei USA 85:8722-8726.
7. Bailey MS, Shipley MT (1993) Astrocyle subtypes in the rat olfactory bulh: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526.
8. 3H-Thvmidine-radiographic studies of neurogenesis in the rat olfactory bulb/Exp Brain Res 50:329-340.
9. Bonfanti L, Theodosis DT (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subcpendymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscicnce 62:291-305.
10. Brunjes PC, Armstrong AM (1996) Apoptosis in the rostral migratory stream of the developing rat. Dev Brain Res 92:219-222.
11. Chao MV (1992) Ncurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593.
12. Chiu K, Greer CA (1996) Immunocytochemical analyses of astrocyte development in the olfactory hulb. Dev Brain Res 95:28-37.
13. Corotto FS, Henegar JA. Maruniak JA (1993) Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci Lett 149:111-114.
14. Corotto FS, Henegar JR. Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulh of the adult mouse. Neuroscicnce 61:739-744.
15. Craig CG. Tropepe V, Morshead CM, Reynolds BA, Weiss S, Van der Kooy D (1996) In vivo growth factor expansion of endogenous suhepcndymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-2658.
16. 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 (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.
17. Doetsch F. Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sei USA 93:14895- 14900.
18. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the suhvenlricular germinal zone in the adult mammalian hrain. J Neurosci 17:5046-5061.
19. Farhman AI (1990) Olfactory neurogenesis: genetic or environmental controls. Trends Neurosci 13:362-365.
20. Forss-Petter S. Danielson PE, Catsicas S. Baltenherg E. Price J. Nerenberg M, Sutcliffe JO (1990) Transgenic mice expressing β-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron 5:187-197.
21. Frazier-Cierpial L, Brunjes PC (1989) Early postnatal cellular proliferation and survival in the olfactory hulh and rostral migratory stream of normal and unilatcrally odor-deprived rats. J Comp Ncurol 289:481-492.
22. Gavrieli Y. Sherman Y. Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
23. Gritti A, Cova L, Parati EA, Galli R. Vescovi AL (1995) Basic fibroblast growth factor supports the proliferation of epidermal growth factor-generated neuronal precursor cells of the adult mouse CNS. Neurosci Lett 185:151-154.
24. Gritti A. Parati EA. Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ. Roisen F. Nickel DD, Vescovi AL (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fihroblast growth factor. J Neurosci 16:1091-1100.
25. Hinds JW (1968) Autoradiographic study of histogencsis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134:287-304.
26. Holeomb JD, Mumm JS, Calof AL (1995) Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro. Dev Biol 172:307-323.
27. Hu HY, Rutishauser U (1996) A septum-derived chemorepulsive factor for migrating olfactory interncuron precursors. Neuron 16:933-940.
28. Jankovski A, Sotchi C (1996) Suhvcntricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Ncurol 371:376-396.
29. Kirschenbaum B, Goldman SA (1995) Brain-derived neurotrophie factor promotes the survival of neurons arising from the adult rat forebrain suhepcndymal zone. Proc Natl Acad Sei USA 92:210-214.
30. 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.
31. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibrohlast growth factor-2 have different effects on neural progenitors in the adult rat hrain. J Neurosci 17:5820-5829.
32. Lin RCS, Matesic DF (1994) Immunohistochemical demonstration of neuron-specific enolase and microtubule-associatcd protein 2 in reactive astrocytes after injury in the adult forcbrain. Neurosciencc 60:11-16.
33. Linden R (1994) The survival of developing neurons: a review of afferent control. Neuroscience 4:671-682.
34. Lois C, Alvarez-Buylla A (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sei USA 90:2074-2077.
35. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
36. Lois C, Garcia-Vcrdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978-981.
37. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the tbrehrain subventricular zone. Neuron 11:173-189.
38. Menezes JRL, Luskin MB (1994) Expression of neuron-specific luhulin defines a novel popuhilion in the prolife rative layers of the developing telencephalon. J Neurosei 14:5399-5416.
39. Mcnezes JRL, Smith CM, Nelson KC, Luskin MB (1995) The division of neuronal progenitor cells during migration in the neonatal mammalian forehrain. Mol Cell Neurosei 6:496-508.
40. Monli-Graziadei AG, Graziadei PPC (1992) Sensory reinnervation after partial removal of the olfactory bulb. J Comp Neurol 316:32-44.
41. Najhaucr J, Leon M (1995) Olfactory experience modulates apoptosis in the developing olfactory bulb. Brain Res 674:245-251.
42. Ono K, Tomasiewicz H, Magnuson T, Rulishauser U (1994) N-CAM mutation inhibits tangential neuronal migration anil is phenoeopicd by enzymatic removal of polysialic acid. Neuron 13:595-609.
43. Reynolds B. Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
44. Richards LJ, Kilpatrick TJ, Bartlett PF (1992) De novo generation of neuronal cells from the adult mouse drain. Proc Nail Acad Sei USA 89:8591-8595.
45. Rougon G, Uuhois C. Buckley N. Magnani JL, Zollinger W (1986) A monoclonal antibody against meningococcus group B pulysuccharid.es distinguishes embryonic from adult N-CAM. J Cell Biol 103:2429-2437.
46. Roussclot 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.
47. Schmechel DE. Marangos PJ (1983) Neuron-specific eiiolasc (NSE): specifie cellular and functional marker for neurons and neuroendocrine cells. In: Current methods in cellular neurohiology (Barker J, McKelvcy J, eds), pp 1-62. New York: Wiley.
48. Sehwob JE, Szumowski KE, Stasky AA (1992) Olfactory sensory neurons are trophically dependent on the olfactory bulb tor their prolonged survival. J Neurosei 12:3890-3919.
49. Slotnick BM. Leonard CM (1975) A stereotaxic atlas of the albino mouse forebrain. Roekville, MD: Dheu.
50. Szele FG, Chesselct MF (1996) Cortical lesions induce an increase in cell number and PSA-NCAM expression in the suhventricular zone of adult rats. J Comp Neurol 368:439-454.
51. Tessier-Lavigne M. Plaezek M. Lumsden AGS, Dodd J, Jessell TM (1988) Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336:775-778.
52. Thomas LB, Gates MA, Steindler DA (1996) Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 17:1-14.
53. 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.
54. Weinstein DE, Burrola P, Kilpatrick TJ (1996) Increased proliferation of precursor cells in the adult rat brain after targeted lesioning. Brain Res 743:11-16.
55. Wichteric H, Garcia-Verdugo JM, Alvarcv-Buylla A (1997) Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18:779-791.
56. Wood KA, Dipasquale B, Youle RJ (1993) In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11:621-632.
57. Yaginuma H, Shiga T, Oppenheim RW (1994) Early developmental patterns and mechanisms of axonal guidance of spinal interneurons in the chick embryo spinal cord. Prog Neurobiol 44:249-278.