Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth

Kenji Hayashi, Atsushi Suzuki, Syu ichi Hirai, Yasuyuki Kurihara, Casper C. Hoogenraad, Shigeo Ohno

    • 21 Citations

    Abstract

    Dendritic spines are postsynaptic structures that receive excitatory synaptic input from presynaptic terminals. Actin and its regulatory proteins play a central role in morphogenesis of dendritic spines. In addition, recent studies have revealed that microtubules are indispensable for the maintenance of mature dendritic spine morphology by stochastically invading dendritic spines and regulating dendritic localization of p140Cap, which is required for actin reorganization. However, the regulatory mechanisms of microtubule dynamics remain poorly understood. Partitioning-defective 1b (PAR1b), a cell polarity-regulating serine/threonine protein kinase, is thought to regulate microtubule dynamics by inhibiting microtubule binding of microtubule-associated proteins. Results from the present study demonstrated that PAR1b participates in the maintenance of mature dendritic spine morphology in mouse hippocampal neurons. Immunofluorescent analysis revealed PAR1b localization in the dendrites, which was concentrated in dendritic spines of mature neurons. PAR1b knock-down cells exhibited decreased mushroom-like dendritic spines, as well as increased filopodia-like dendritic protrusions, with no effect on the number of protrusions. Live imaging of microtubule plus-end tracking proteins directly revealed decreases in distance and duration of microtubule growth following PAR1b knockdown in a neuroblastoma cell line and in dendrites of hippocampal neurons. In addition, reduced accumulation of GFP-p140Cap in dendritic protrusions was confirmed inPAR1b knock-down neurons. In conclusion, the present results suggested a novel function for PAR1b in the maintenance of mature dendritic spine morphology by regulating microtubule growth and the accumulation of p140Cap in dendritic spines. © 2011 the authors.

    Original languageEnglish
    Pages (from-to)12094-12103
    Number of pages10
    JournalJournal of Neuroscience
    Volume31
    Issue number34
    DOIs
    StatePublished - 2011 Aug 24

    Fingerprint

    Dendritic Spines
    Microtubules
    Neurons
    Dendrites
    Actins
    Proteins
    Cell Polarity
    Pseudopodia
    Microtubule-Associated Proteins
    Agaricales
    Protein-Serine-Threonine Kinases
    Presynaptic Terminals
    Neuroblastoma
    Morphogenesis
    Cell Line

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth. / Hayashi, Kenji; Suzuki, Atsushi; Hirai, Syu ichi; Kurihara, Yasuyuki; Hoogenraad, Casper C.; Ohno, Shigeo.

    In: Journal of Neuroscience, Vol. 31, No. 34, 24.08.2011, p. 12094-12103.

    Research output: Contribution to journalArticle

    Hayashi, Kenji; Suzuki, Atsushi; Hirai, Syu ichi; Kurihara, Yasuyuki; Hoogenraad, Casper C.; Ohno, Shigeo / Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth.

    In: Journal of Neuroscience, Vol. 31, No. 34, 24.08.2011, p. 12094-12103.

    Research output: Contribution to journalArticle

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    author = "Kenji Hayashi and Atsushi Suzuki and Hirai, {Syu ichi} and Yasuyuki Kurihara and Hoogenraad, {Casper C.} and Shigeo Ohno",
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    AU - Suzuki,Atsushi

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    AU - Hoogenraad,Casper C.

    AU - Ohno,Shigeo

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    N2 - Dendritic spines are postsynaptic structures that receive excitatory synaptic input from presynaptic terminals. Actin and its regulatory proteins play a central role in morphogenesis of dendritic spines. In addition, recent studies have revealed that microtubules are indispensable for the maintenance of mature dendritic spine morphology by stochastically invading dendritic spines and regulating dendritic localization of p140Cap, which is required for actin reorganization. However, the regulatory mechanisms of microtubule dynamics remain poorly understood. Partitioning-defective 1b (PAR1b), a cell polarity-regulating serine/threonine protein kinase, is thought to regulate microtubule dynamics by inhibiting microtubule binding of microtubule-associated proteins. Results from the present study demonstrated that PAR1b participates in the maintenance of mature dendritic spine morphology in mouse hippocampal neurons. Immunofluorescent analysis revealed PAR1b localization in the dendrites, which was concentrated in dendritic spines of mature neurons. PAR1b knock-down cells exhibited decreased mushroom-like dendritic spines, as well as increased filopodia-like dendritic protrusions, with no effect on the number of protrusions. Live imaging of microtubule plus-end tracking proteins directly revealed decreases in distance and duration of microtubule growth following PAR1b knockdown in a neuroblastoma cell line and in dendrites of hippocampal neurons. In addition, reduced accumulation of GFP-p140Cap in dendritic protrusions was confirmed inPAR1b knock-down neurons. In conclusion, the present results suggested a novel function for PAR1b in the maintenance of mature dendritic spine morphology by regulating microtubule growth and the accumulation of p140Cap in dendritic spines. © 2011 the authors.

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