Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons

Mari Sajo, Hiroki Sugiyama, Hideaki Yamamoto, Takashi Tanii, Norio Matsuki, Yuji Ikegaya, Ryuta Koyama

    Research output: Contribution to journalArticle

    7 Citations (Scopus)

    Abstract

    Hippocampal granule cells (GCs) are generated throughout the lifetime and are properly incorporated into the innermost region of the granule cell layer (GCL). Hypotheses for the well-regulated lamination of newly generated GCs suggest that polysialic acid (PSA) is present on the GC surface to modulate GC-to-GC interactions, regulating the process of GC migration; however, direct evidence of this involvement is lacking. We show that PSA facilitates the migration of newly generated GCs and that the activity of N-acetyl-α-neuraminidase 1 (NEU1, sialidase 1) cleaves PSA from immature GCs, terminating their migration in the innermost GCL. Developing a migration assay of immature GCs in vitro, we found that the pharmacological depletion of PSA prevents the migration of GCs, whereas the inhibition of PSA degradation with a neuraminidase inhibitor accelerates this migration. We found that NEU1 is highly expressed in immature GCs. The knockdown of NEU1 in newly generated GCs in vivo increased PSA presence on these cells, and attenuated the proper termination of GC migration in the innermost GCL. In conclusion, this study identifies a novel mechanism that underlies the proper lamination of newly generated GCs through the modulation of PSA presence by neuronal NEU1.

    Original languageEnglish
    Article numbere0146398
    JournalPLoS One
    Volume11
    Issue number1
    DOIs
    Publication statusPublished - 2016 Jan 5

    Fingerprint

    sialidase
    Neuraminidase
    Neurons
    granules
    neurons
    Degradation
    degradation
    acids
    cells
    Cell Movement
    Corrosion inhibitors
    polysialic acid
    immatures
    Assays
    cell movement
    Cells
    Modulation
    Cell Communication

    ASJC Scopus subject areas

    • Agricultural and Biological Sciences(all)
    • Biochemistry, Genetics and Molecular Biology(all)
    • Medicine(all)

    Cite this

    Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons. / Sajo, Mari; Sugiyama, Hiroki; Yamamoto, Hideaki; Tanii, Takashi; Matsuki, Norio; Ikegaya, Yuji; Koyama, Ryuta.

    In: PLoS One, Vol. 11, No. 1, e0146398, 05.01.2016.

    Research output: Contribution to journalArticle

    Sajo, Mari ; Sugiyama, Hiroki ; Yamamoto, Hideaki ; Tanii, Takashi ; Matsuki, Norio ; Ikegaya, Yuji ; Koyama, Ryuta. / Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons. In: PLoS One. 2016 ; Vol. 11, No. 1.
    @article{b4bcc2962aca421481970a59770ec741,
    title = "Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons",
    abstract = "Hippocampal granule cells (GCs) are generated throughout the lifetime and are properly incorporated into the innermost region of the granule cell layer (GCL). Hypotheses for the well-regulated lamination of newly generated GCs suggest that polysialic acid (PSA) is present on the GC surface to modulate GC-to-GC interactions, regulating the process of GC migration; however, direct evidence of this involvement is lacking. We show that PSA facilitates the migration of newly generated GCs and that the activity of N-acetyl-α-neuraminidase 1 (NEU1, sialidase 1) cleaves PSA from immature GCs, terminating their migration in the innermost GCL. Developing a migration assay of immature GCs in vitro, we found that the pharmacological depletion of PSA prevents the migration of GCs, whereas the inhibition of PSA degradation with a neuraminidase inhibitor accelerates this migration. We found that NEU1 is highly expressed in immature GCs. The knockdown of NEU1 in newly generated GCs in vivo increased PSA presence on these cells, and attenuated the proper termination of GC migration in the innermost GCL. In conclusion, this study identifies a novel mechanism that underlies the proper lamination of newly generated GCs through the modulation of PSA presence by neuronal NEU1.",
    author = "Mari Sajo and Hiroki Sugiyama and Hideaki Yamamoto and Takashi Tanii and Norio Matsuki and Yuji Ikegaya and Ryuta Koyama",
    year = "2016",
    month = "1",
    day = "5",
    doi = "10.1371/journal.pone.0146398",
    language = "English",
    volume = "11",
    journal = "PLoS One",
    issn = "1932-6203",
    publisher = "Public Library of Science",
    number = "1",

    }

    TY - JOUR

    T1 - Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons

    AU - Sajo, Mari

    AU - Sugiyama, Hiroki

    AU - Yamamoto, Hideaki

    AU - Tanii, Takashi

    AU - Matsuki, Norio

    AU - Ikegaya, Yuji

    AU - Koyama, Ryuta

    PY - 2016/1/5

    Y1 - 2016/1/5

    N2 - Hippocampal granule cells (GCs) are generated throughout the lifetime and are properly incorporated into the innermost region of the granule cell layer (GCL). Hypotheses for the well-regulated lamination of newly generated GCs suggest that polysialic acid (PSA) is present on the GC surface to modulate GC-to-GC interactions, regulating the process of GC migration; however, direct evidence of this involvement is lacking. We show that PSA facilitates the migration of newly generated GCs and that the activity of N-acetyl-α-neuraminidase 1 (NEU1, sialidase 1) cleaves PSA from immature GCs, terminating their migration in the innermost GCL. Developing a migration assay of immature GCs in vitro, we found that the pharmacological depletion of PSA prevents the migration of GCs, whereas the inhibition of PSA degradation with a neuraminidase inhibitor accelerates this migration. We found that NEU1 is highly expressed in immature GCs. The knockdown of NEU1 in newly generated GCs in vivo increased PSA presence on these cells, and attenuated the proper termination of GC migration in the innermost GCL. In conclusion, this study identifies a novel mechanism that underlies the proper lamination of newly generated GCs through the modulation of PSA presence by neuronal NEU1.

    AB - Hippocampal granule cells (GCs) are generated throughout the lifetime and are properly incorporated into the innermost region of the granule cell layer (GCL). Hypotheses for the well-regulated lamination of newly generated GCs suggest that polysialic acid (PSA) is present on the GC surface to modulate GC-to-GC interactions, regulating the process of GC migration; however, direct evidence of this involvement is lacking. We show that PSA facilitates the migration of newly generated GCs and that the activity of N-acetyl-α-neuraminidase 1 (NEU1, sialidase 1) cleaves PSA from immature GCs, terminating their migration in the innermost GCL. Developing a migration assay of immature GCs in vitro, we found that the pharmacological depletion of PSA prevents the migration of GCs, whereas the inhibition of PSA degradation with a neuraminidase inhibitor accelerates this migration. We found that NEU1 is highly expressed in immature GCs. The knockdown of NEU1 in newly generated GCs in vivo increased PSA presence on these cells, and attenuated the proper termination of GC migration in the innermost GCL. In conclusion, this study identifies a novel mechanism that underlies the proper lamination of newly generated GCs through the modulation of PSA presence by neuronal NEU1.

    UR - http://www.scopus.com/inward/record.url?scp=84953911433&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84953911433&partnerID=8YFLogxK

    U2 - 10.1371/journal.pone.0146398

    DO - 10.1371/journal.pone.0146398

    M3 - Article

    VL - 11

    JO - PLoS One

    JF - PLoS One

    SN - 1932-6203

    IS - 1

    M1 - e0146398

    ER -