Neurogenesis and Neuronal Migration in the Neonatal Rat Forebrain Anterior Subventricular Zone Do Not Require GFAP-Positive Astrocytes

A prolific neuronal progenitor cell population in the anterior portion of the neonatal rat forebrain subventricular zone, the SVZa, is specialized for the production of olfactory bulb interneurons. At all ages, SVZa-derived cells traverse a tangential migratory pathway, the rostral migratory stream...

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Published inDevelopmental biology Vol. 216; no. 2; pp. 622 - 634
Main Authors Law, Alick K.T., Pencea, Viorica, Buck, Charles R., Luskin, Marla B.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.12.1999
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Abstract A prolific neuronal progenitor cell population in the anterior portion of the neonatal rat forebrain subventricular zone, the SVZa, is specialized for the production of olfactory bulb interneurons. At all ages, SVZa-derived cells traverse a tangential migratory pathway, the rostral migratory stream (RMS), while en route to the olfactory bulb. Unlike other neuronal progenitor cells of the forebrain, migrating progeny of SVZa progenitors express neuronal-specific proteins and continue to divide into adulthood. Recent studies indicate that in the adult, migrating SVZa-derived cells are ensheathed by astrocytes, although the function of these astrocytes has not been determined. To explore the possible role(s) of astrocytes in the rat SVZa and RMS, we examined the expression of astroglial-specific genes in the postnatal SVZa and RMS using RT-PCR, in situ hybridization, and immunohistochemistry during (Postnatal Days 1–10) and after the period of peak olfactory bulb interneuron generation. We also examined the expression of neuronal-specific genes throughout the rostral-caudal extent of the postnatal subventricular zone to determine if differential cell type-specific gene expression could distinguish the neurogenic SVZa as a region distinct from the remainder of the SVZ. We found little to no astrocyte-specific gene expression in the P0-P7 SVZa, although the neuron-specific isoforms of tubulin (Tα1 and β-III tubulin) were expressed abundantly in the SVZa and RMS. In contrast, astrocyte-specific genes were strongly expressed in the SVZ posterior to the SVZa. GFAP expressions begins to appear in some restricted areas of the rostral migratory stream after the first postnatal week. These data suggest that astroglia are not involved in the generation or migration of most olfactory bulb interneurons. Moreover, the scarcity of glial markers in the neonatal SVZa indicates that the forebrain subventricular zone includes a distinct neurogenic anterior region containing predominantly committed neuronal progenitor cells.
AbstractList A prolific neuronal progenitor cell population in the anterior portion of the neonatal rat forebrain subventricular zone, the SVZa, is specialized for the production of olfactory bulb interneurons. At all ages, SVZa-derived cells traverse a tangential migratory pathway, the rostral migratory stream (RMS), while en route to the olfactory bulb. Unlike other neuronal progenitor cells of the forebrain, migrating progeny of SVZa progenitors express neuronal-specific proteins and continue to divide into adulthood. Recent studies indicate that in the adult, migrating SVZa-derived cells are ensheathed by astrocytes, although the function of these astrocytes has not been determined. To explore the possible role(s) of astrocytes in the rat SVZa and RMS, we examined the expression of astroglial-specific genes in the postnatal SVZa and RMS using RT-PCR, in situ hybridization, and immunohistochemistry during (Postnatal Days 1-10) and after the period of peak olfactory bulb interneuron generation. We also examined the expression of neuronal-specific genes throughout the rostral-caudal extent of the postnatal subventricular zone to determine if differential cell type-specific gene expression could distinguish the neurogenic SVZa as a region distinct from the remainder of the SVZ. We found little to no astrocyte-specific gene expression in the P0-P7 SVZa, although the neuron-specific isoforms of tubulin (T alpha 1 and beta-III tubulin) were expressed abundantly in the SVZa and RMS. In contrast, astrocyte-specific genes were strongly expressed in the SVZ posterior to the SVZa. GFAP expressions begins to appear in some restricted areas of the rostral migratory stream after the first postnatal week. These data suggest that astroglia are not involved in the generation or migration of most olfactory bulb interneurons. Moreover, the scarcity of glial markers in the neonatal SVZa indicates that the forebrain subventricular zone includes a distinct neurogenic anterior region containing predominantly committed neuronal progenitor cells.
A prolific neuronal progenitor cell population in the anterior portion of the neonatal rat forebrain subventricular zone, the SVZa, is specialized for the production of olfactory bulb interneurons. At all ages, SVZa-derived cells traverse a tangential migratory pathway, the rostral migratory stream (RMS), while en route to the olfactory bulb. Unlike other neuronal progenitor cells of the forebrain, migrating progeny of SVZa progenitors express neuronal-specific proteins and continue to divide into adulthood. Recent studies indicate that in the adult, migrating SVZa-derived cells are ensheathed by astrocytes, although the function of these astrocytes has not been determined. To explore the possible role(s) of astrocytes in the rat SVZa and RMS, we examined the expression of astroglial-specific genes in the postnatal SVZa and RMS using RT-PCR, in situ hybridization, and immunohistochemistry during (Postnatal Days 1–10) and after the period of peak olfactory bulb interneuron generation. We also examined the expression of neuronal-specific genes throughout the rostral-caudal extent of the postnatal subventricular zone to determine if differential cell type-specific gene expression could distinguish the neurogenic SVZa as a region distinct from the remainder of the SVZ. We found little to no astrocyte-specific gene expression in the P0-P7 SVZa, although the neuron-specific isoforms of tubulin (Tα1 and β-III tubulin) were expressed abundantly in the SVZa and RMS. In contrast, astrocyte-specific genes were strongly expressed in the SVZ posterior to the SVZa. GFAP expressions begins to appear in some restricted areas of the rostral migratory stream after the first postnatal week. These data suggest that astroglia are not involved in the generation or migration of most olfactory bulb interneurons. Moreover, the scarcity of glial markers in the neonatal SVZa indicates that the forebrain subventricular zone includes a distinct neurogenic anterior region containing predominantly committed neuronal progenitor cells.
Author Buck, Charles R.
Pencea, Viorica
Luskin, Marla B.
Law, Alick K.T.
Author_xml – sequence: 1
  givenname: Alick K.T.
  surname: Law
  fullname: Law, Alick K.T.
  organization: Department of Physiology, Emory University School of Medicine, Atlanta, Georgia, 30322
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  givenname: Viorica
  surname: Pencea
  fullname: Pencea, Viorica
  organization: Department of Cell Biology, Emory University School of Medicine, Atlanta, Georgia, 30322
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  givenname: Charles R.
  surname: Buck
  fullname: Buck, Charles R.
  organization: Department of Physiology, Emory University School of Medicine, Atlanta, Georgia, 30322
– sequence: 4
  givenname: Marla B.
  surname: Luskin
  fullname: Luskin, Marla B.
  organization: Department of Cell Biology, Emory University School of Medicine, Atlanta, Georgia, 30322
BackLink https://www.ncbi.nlm.nih.gov/pubmed/10642797$$D View this record in MEDLINE/PubMed
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Keywords neurogenesis
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olfactory bulb
forebrain
progenitor cell
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Snippet A prolific neuronal progenitor cell population in the anterior portion of the neonatal rat forebrain subventricular zone, the SVZa, is specialized for the...
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SubjectTerms Animals
Animals, Newborn - growth & development
Astrocytes - metabolism
Biomarkers
Brain - growth & development
Cell Differentiation
Cell Movement
development
forebrain
Gene Expression Regulation, Developmental
Immunohistochemistry
In Situ Hybridization
Microscopy, Fluorescence
neurogenesis
Neurons - metabolism
olfactory bulb
progenitor cell
Rats
Reverse Transcriptase Polymerase Chain Reaction
RNA, Messenger - metabolism
Title Neurogenesis and Neuronal Migration in the Neonatal Rat Forebrain Anterior Subventricular Zone Do Not Require GFAP-Positive Astrocytes
URI https://dx.doi.org/10.1006/dbio.1999.9498
https://www.ncbi.nlm.nih.gov/pubmed/10642797
https://search.proquest.com/docview/69417651
Volume 216
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