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PMID: 10066270 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

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

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 19 ·No. 6 ·1999-03-15 ·Pages 2171-80

Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A

Abstract

Neurons continue to be born in the subventricular zone (SVZ) of the lateral ventricles of adult mice. These cells migrate as a network of chains through the SVZ and the rostral migratory stream (RMS) into the olfactory bulb (OB), where they differentiate into mature neurons. The OB is the only known target for these neuronal precursors. Here, we show that, after elimination of the OB, the SVZ and RMS persist and become dramatically larger. The proportion of dividing [bromodeoxyuridine (BrdU)-labeled] or dying (pyknotic or terminal deoxynucleotidyl transferase-mediated biotinylated UTP nick end-labeled) cells in the RMS was not significantly affected at 3 d or 3 weeks after bulbectomy (OBX). However, by 3 months after OBX, the percentage of BrdU-labeled cells in the RMS decreased by half and that of dying cells doubled. Surprisingly, the rostral migration of precursors continued along the RMS after OBX. This was demonstrated by focal microinjections of BrdU and grafts of SVZ cells carrying LacZ under the control of a neuron-specific promoter gene. Results indicate that the OB is not essential for proliferation and the directional migration of SVZ precursors.

MeSH Terms
Animals Cell Division/physiology Cell Movement/physiology Cell Transplantation Cerebral Ventricles/cytology Male Mice Mice, Inbred Strains Mice, Transgenic/genetics Nerve Net/physiology Neurons/cytology,enzymology,physiology Olfactory Bulb/physiology Phosphopyruvate Hydratase/genetics,metabolism Stem Cells/cytology,physiology Time Factors
Chemicals
Phosphopyruvate Hydratase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kirschenbaum B
The Rockefeller University, New York, New York 10021, USA.
Doetsch F
Lois C
Alvarez-Buylla A
References (55)
55 references, click to expand
  1. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
    J Cell Biol. 1992 Nov;119(3):493-501 PMID: 1400587
  2. N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid.
    Neuron. 1994 Sep;13(3):595-609 PMID: 7917293
  3. Early developmental patterns and mechanisms of axonal guidance of spinal interneurons in the chick embryo spinal cord.
    Prog Neurobiol. 1994 Oct;44(3):249-78 PMID: 7886227
  4. Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival.
    J Neurosci. 1992 Oct;12(10):3896-919 PMID: 1403089
  5. Basic fibroblast growth factor supports the proliferation of epidermal growth factor-generated neuronal precursor cells of the adult mouse CNS.
    Neurosci Lett. 1995 Feb 13;185(3):151-4 PMID: 7753479
  6. Olfactory experience modulated apoptosis in the developing olfactory bulb.
    Brain Res. 1995 Mar 20;674(2):245-51 PMID: 7796103
  7. Immunohistochemical demonstration of neuron-specific enolase and microtubule-associated protein 2 in reactive astrocytes after injury in the adult forebrain.
    Neuroscience. 1994 May;60(1):11-6 PMID: 8052405
  8. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb.
    Exp Brain Res. 1983;50(2-3):329-40 PMID: 6641865
  9. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone.
    Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):210-4 PMID: 7816819
  10. Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation.
    J Comp Neurol. 1996 Jul 29;371(3):376-96 PMID: 8842894
  11. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway.
    Glia. 1996 May;17(1):1-14 PMID: 8723838
  12. Mechanism of migration of olfactory bulb interneurons.
    Semin Cell Dev Biol. 1997 Apr;8(2):207-13 PMID: 15001097
  13. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor.
    J Neurosci. 1996 Feb 1;16(3):1091-100 PMID: 8558238
  14. Long-distance neuronal migration in the adult mammalian brain.
    Science. 1994 May 20;264(5162):1145-8 PMID: 8178174
  15. De novo generation of neuronal cells from the adult mouse brain.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8591-5 PMID: 1528866
  16. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors.
    J Neurosci. 1995 Aug;15(8):5765-78 PMID: 7643217
  17. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2429-37 PMID: 3536966
  18. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain.
    J Neurosci. 1997 Jul 1;17(13):5046-61 PMID: 9185542
  19. Neurotrophin receptors: a window into neuronal differentiation.
    Neuron. 1992 Oct;9(4):583-93 PMID: 1327010
  20. Monoclonal antibody reveals radial glia in adult avian brain.
    J Comp Neurol. 1987 Oct 8;264(2):159-70 PMID: 2445794
  21. Network of tangential pathways for neuronal migration in adult mammalian brain.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14895-900 PMID: 8962152
  22. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain.
    Mol Cell Neurosci. 1995 Dec;6(6):496-508 PMID: 8742267
  23. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system.
    Science. 1992 Mar 27;255(5052):1707-10 PMID: 1553558
  24. The survival of developing neurons: a review of afferent control.
    Neuroscience. 1994 Feb;58(4):671-82 PMID: 8190251
  25. Sensory reinnervation after partial removal of the olfactory bulb.
    J Comp Neurol. 1992 Feb 1;316(1):32-44 PMID: 1573050
  26. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control.
    Neuron. 1990 Aug;5(2):187-97 PMID: 2116814
  27. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2074-7 PMID: 8446631
  28. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain.
    J Neurosci. 1996 Apr 15;16(8):2649-58 PMID: 8786441
  29. Direct evidence for homotypic, glia-independent neuronal migration.
    Neuron. 1997 May;18(5):779-91 PMID: 9182802
  30. Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer.
    J Comp Neurol. 1987 Apr 1;258(1):112-24 PMID: 3571532
  31. Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats.
    J Comp Neurol. 1989 Nov 15;289(3):481-92 PMID: 2808782
  32. Apoptosis in the neuronal lineage of the mouse olfactory epithelium: regulation in vivo and in vitro.
    Dev Biol. 1995 Nov;172(1):307-23 PMID: 7589810
  33. Olfactory neurogenesis: genetic or environmental controls?
    Trends Neurosci. 1990 Sep;13(9):362-5 PMID: 1699323
  34. Immunocytochemical analyses of astrocyte development in the olfactory bulb.
    Brain Res Dev Brain Res. 1996 Aug 20;95(1):28-37 PMID: 8873973
  35. Chain migration of neuronal precursors.
    Science. 1996 Feb 16;271(5251):978-81 PMID: 8584933
  36. Simple microcomputer system for mapping tissue sections with the light microscope.
    J Neurosci Methods. 1988 Sep;25(2):165-73 PMID: 3172826
  37. Chemotropic guidance of developing axons in the mammalian central nervous system.
    Nature. 1988 Dec 22-29;336(6201):775-8 PMID: 3205306
  38. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone.
    Neuron. 1993 Jul;11(1):173-89 PMID: 8338665
  39. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia.
    J Comp Neurol. 1968 Nov;134(3):287-304 PMID: 5721256
  40. Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system.
    Neuron. 1993 Dec;11(6):1163-74 PMID: 8274281
  41. 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. 1969 Dec;137(4):433-57 PMID: 5361244
  42. Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning.
    Proc Natl Acad Sci U S A. 1988 Nov;85(22):8722-6 PMID: 3186755
  43. 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. 1994 Sep;62(1):291-305 PMID: 7816207
  44. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning.
    Nature. 1994 Feb 3;367(6462):455-9 PMID: 8107803
  45. Cortical lesions induce an increase in cell number and PSA-NCAM expression in the subventricular zone of adult rats.
    J Comp Neurol. 1996 May 06;368(3):439-54 PMID: 8725350
  46. Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse.
    Neuroscience. 1994 Aug;61(4):739-44 PMID: 7838373
  47. Increased proliferation of precursor cells in the adult rat brain after targeted lesioning.
    Brain Res. 1996 Dec 16;743(1-2):11-6 PMID: 9017224
  48. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain.
    J Neurosci. 1997 Aug 1;17(15):5820-9 PMID: 9221780
  49. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice.
    J Comp Neurol. 1995 Jan 2;351(1):51-61 PMID: 7896939
  50. Apoptosis in the rostral migratory stream of the developing rat.
    Brain Res Dev Brain Res. 1996 Apr 30;92(2):219-22 PMID: 8738129
  51. Neurogenesis persists in the subependymal layer of the adult mouse brain.
    Neurosci Lett. 1993 Jan 12;149(2):111-4 PMID: 8474679
  52. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon.
    J Neurosci. 1994 Sep;14(9):5399-416 PMID: 8083744
  53. In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum.
    Neuron. 1993 Oct;11(4):621-32 PMID: 8398151
  54. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution.
    J Comp Neurol. 1993 Feb 22;328(4):501-26 PMID: 8429132
  55. A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors.
    Neuron. 1996 May;16(5):933-40 PMID: 8630251
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1999-03-15
Pages
2171-80
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782582
Subset
IM
Grants
NINDS NIH HHS · R01 NS028478 · United States
NINDS NIH HHS · NS28478 · United States
NIDCD NIH HHS · DC03046 · United States
NICHD NIH HHS · HD32116 · United States
NICHD NIH HHS · R37 HD032116 · United States
NINDS NIH HHS · R37 NS028478 · United States
NICHD NIH HHS · R01 HD032116 · United States
External Links
PubMed source PMC Full Text View journal details
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