Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors

C. B. Chambers, Y. Peng, H. Nguyen, N. Gaiano, Gordon Fishell, J. S. Nye

    Research output: Contribution to journalArticle

    Abstract

    The olfactory bulb, neocortex and archicortex arise from a common pool of progenitors in the dorsal telencephalon. We studied the consequences of supplying excess Notch1 signal in vivo on the cellular and regional destinies of telencephalic precursors using bicistronic replication defective retroviruses. After ventricular injections mid-neurogenesis (E14.5), activated Notch1 retrovirus markedly inhibited the generation of neurons from telencephalic precursors, delayed the emergence of cells from the subventricular zone (SVZ), and produced an augmentation of glial progeny in the neo- and archicortex. However, activated Notch1 had a distinct effect on the progenitors of the olfactory bulb, markedly reducing the numbers of cells of any type that migrated there. To elucidate the mechanism of the cell fate changes elicited by Notch1 signals in the cortical regions, short- and long-term cultures of E14.5 telencephalic progenitors were examined. These studies reveal that activated Notch1 elicits a cessation of proliferation that coincides with an inhibition of the generation of neurons. Later, during gliogenesis, activated Notch1 triggers a rapid cellular proliferation with a significant increase in the generation of cells expressing GFAP. To examine the generation of cells destined for the olfactory bulb, we used stereotaxic injections into the early postnatal anterior subventricular zone (SVZa). We observed that precursors of the olfactory bulb responded to Notch signals by remaining quiescent and failing to give rise to differentiated progeny of any type, unlike cortical precursor cells, which generated glia instead of neurons. These data show that forebrain precursors vary in their response to Notch signals according to spatial and temporal cues, and that Notch signals influence the composition of forebrain regions by modulating the rate of proliferation of neural precursor cells.

    Original languageEnglish (US)
    Pages (from-to)689-702
    Number of pages14
    JournalDevelopment
    Volume128
    Issue number5
    StatePublished - Apr 2 2001

    Fingerprint

    Prosencephalon
    Telencephalon
    Olfactory Bulb
    Lateral Ventricles
    Neocortex
    Retroviridae
    Neurons
    Neuroglia
    Injections
    Neurogenesis
    Cues
    Cell Count
    Cell Proliferation

    Keywords

    • Gliogenesis
    • Mouse
    • Neural progenitor
    • Neurogenesis
    • Neurosphere
    • Stem cell
    • Subventricular zone
    • Telencephalon

    ASJC Scopus subject areas

    • Molecular Biology
    • Developmental Biology

    Cite this

    Chambers, C. B., Peng, Y., Nguyen, H., Gaiano, N., Fishell, G., & Nye, J. S. (2001). Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development, 128(5), 689-702.

    Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. / Chambers, C. B.; Peng, Y.; Nguyen, H.; Gaiano, N.; Fishell, Gordon; Nye, J. S.

    In: Development, Vol. 128, No. 5, 02.04.2001, p. 689-702.

    Research output: Contribution to journalArticle

    Chambers, CB, Peng, Y, Nguyen, H, Gaiano, N, Fishell, G & Nye, JS 2001, 'Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors', Development, vol. 128, no. 5, pp. 689-702.
    Chambers CB, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye JS. Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development. 2001 Apr 2;128(5):689-702.
    Chambers, C. B. ; Peng, Y. ; Nguyen, H. ; Gaiano, N. ; Fishell, Gordon ; Nye, J. S. / Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. In: Development. 2001 ; Vol. 128, No. 5. pp. 689-702.
    @article{aaf1649ab60b44fa9364ea70145b7378,
    title = "Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors",
    abstract = "The olfactory bulb, neocortex and archicortex arise from a common pool of progenitors in the dorsal telencephalon. We studied the consequences of supplying excess Notch1 signal in vivo on the cellular and regional destinies of telencephalic precursors using bicistronic replication defective retroviruses. After ventricular injections mid-neurogenesis (E14.5), activated Notch1 retrovirus markedly inhibited the generation of neurons from telencephalic precursors, delayed the emergence of cells from the subventricular zone (SVZ), and produced an augmentation of glial progeny in the neo- and archicortex. However, activated Notch1 had a distinct effect on the progenitors of the olfactory bulb, markedly reducing the numbers of cells of any type that migrated there. To elucidate the mechanism of the cell fate changes elicited by Notch1 signals in the cortical regions, short- and long-term cultures of E14.5 telencephalic progenitors were examined. These studies reveal that activated Notch1 elicits a cessation of proliferation that coincides with an inhibition of the generation of neurons. Later, during gliogenesis, activated Notch1 triggers a rapid cellular proliferation with a significant increase in the generation of cells expressing GFAP. To examine the generation of cells destined for the olfactory bulb, we used stereotaxic injections into the early postnatal anterior subventricular zone (SVZa). We observed that precursors of the olfactory bulb responded to Notch signals by remaining quiescent and failing to give rise to differentiated progeny of any type, unlike cortical precursor cells, which generated glia instead of neurons. These data show that forebrain precursors vary in their response to Notch signals according to spatial and temporal cues, and that Notch signals influence the composition of forebrain regions by modulating the rate of proliferation of neural precursor cells.",
    keywords = "Gliogenesis, Mouse, Neural progenitor, Neurogenesis, Neurosphere, Stem cell, Subventricular zone, Telencephalon",
    author = "Chambers, {C. B.} and Y. Peng and H. Nguyen and N. Gaiano and Gordon Fishell and Nye, {J. S.}",
    year = "2001",
    month = "4",
    day = "2",
    language = "English (US)",
    volume = "128",
    pages = "689--702",
    journal = "Development (Cambridge)",
    issn = "0950-1991",
    publisher = "Company of Biologists Ltd",
    number = "5",

    }

    TY - JOUR

    T1 - Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors

    AU - Chambers, C. B.

    AU - Peng, Y.

    AU - Nguyen, H.

    AU - Gaiano, N.

    AU - Fishell, Gordon

    AU - Nye, J. S.

    PY - 2001/4/2

    Y1 - 2001/4/2

    N2 - The olfactory bulb, neocortex and archicortex arise from a common pool of progenitors in the dorsal telencephalon. We studied the consequences of supplying excess Notch1 signal in vivo on the cellular and regional destinies of telencephalic precursors using bicistronic replication defective retroviruses. After ventricular injections mid-neurogenesis (E14.5), activated Notch1 retrovirus markedly inhibited the generation of neurons from telencephalic precursors, delayed the emergence of cells from the subventricular zone (SVZ), and produced an augmentation of glial progeny in the neo- and archicortex. However, activated Notch1 had a distinct effect on the progenitors of the olfactory bulb, markedly reducing the numbers of cells of any type that migrated there. To elucidate the mechanism of the cell fate changes elicited by Notch1 signals in the cortical regions, short- and long-term cultures of E14.5 telencephalic progenitors were examined. These studies reveal that activated Notch1 elicits a cessation of proliferation that coincides with an inhibition of the generation of neurons. Later, during gliogenesis, activated Notch1 triggers a rapid cellular proliferation with a significant increase in the generation of cells expressing GFAP. To examine the generation of cells destined for the olfactory bulb, we used stereotaxic injections into the early postnatal anterior subventricular zone (SVZa). We observed that precursors of the olfactory bulb responded to Notch signals by remaining quiescent and failing to give rise to differentiated progeny of any type, unlike cortical precursor cells, which generated glia instead of neurons. These data show that forebrain precursors vary in their response to Notch signals according to spatial and temporal cues, and that Notch signals influence the composition of forebrain regions by modulating the rate of proliferation of neural precursor cells.

    AB - The olfactory bulb, neocortex and archicortex arise from a common pool of progenitors in the dorsal telencephalon. We studied the consequences of supplying excess Notch1 signal in vivo on the cellular and regional destinies of telencephalic precursors using bicistronic replication defective retroviruses. After ventricular injections mid-neurogenesis (E14.5), activated Notch1 retrovirus markedly inhibited the generation of neurons from telencephalic precursors, delayed the emergence of cells from the subventricular zone (SVZ), and produced an augmentation of glial progeny in the neo- and archicortex. However, activated Notch1 had a distinct effect on the progenitors of the olfactory bulb, markedly reducing the numbers of cells of any type that migrated there. To elucidate the mechanism of the cell fate changes elicited by Notch1 signals in the cortical regions, short- and long-term cultures of E14.5 telencephalic progenitors were examined. These studies reveal that activated Notch1 elicits a cessation of proliferation that coincides with an inhibition of the generation of neurons. Later, during gliogenesis, activated Notch1 triggers a rapid cellular proliferation with a significant increase in the generation of cells expressing GFAP. To examine the generation of cells destined for the olfactory bulb, we used stereotaxic injections into the early postnatal anterior subventricular zone (SVZa). We observed that precursors of the olfactory bulb responded to Notch signals by remaining quiescent and failing to give rise to differentiated progeny of any type, unlike cortical precursor cells, which generated glia instead of neurons. These data show that forebrain precursors vary in their response to Notch signals according to spatial and temporal cues, and that Notch signals influence the composition of forebrain regions by modulating the rate of proliferation of neural precursor cells.

    KW - Gliogenesis

    KW - Mouse

    KW - Neural progenitor

    KW - Neurogenesis

    KW - Neurosphere

    KW - Stem cell

    KW - Subventricular zone

    KW - Telencephalon

    UR - http://www.scopus.com/inward/record.url?scp=0035090226&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=0035090226&partnerID=8YFLogxK

    M3 - Article

    VL - 128

    SP - 689

    EP - 702

    JO - Development (Cambridge)

    JF - Development (Cambridge)

    SN - 0950-1991

    IS - 5

    ER -