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Identification of the growth cone as a probe and driver of neuronal migration in the injured brain

Author

Listed:
  • Chikako Nakajima

    (Nagoya City University Graduate School of Medical Sciences)

  • Masato Sawada

    (Nagoya City University Graduate School of Medical Sciences
    Division of Neural Development and Regeneration, National Institute for Physiological Sciences)

  • Erika Umeda

    (Nagoya City University Graduate School of Medical Sciences)

  • Yuma Takagi

    (Nagoya City University Graduate School of Medical Sciences)

  • Norihiko Nakashima

    (Nagoya City University Graduate School of Medical Sciences)

  • Kazuya Kuboyama

    (Nagoya City University Graduate School of Medical Sciences)

  • Naoko Kaneko

    (Nagoya City University Graduate School of Medical Sciences
    Doshisha University)

  • Satoaki Yamamoto

    (Nagoya City University Graduate School of Medical Sciences)

  • Haruno Nakamura

    (Nagoya City University Graduate School of Medical Sciences)

  • Naoki Shimada

    (Research and Development Center, The Japan Wool Textile Co., Ltd.)

  • Koichiro Nakamura

    (Medical Device Department, Nikke Medical Co., Ltd.)

  • Kumiko Matsuno

    (Research and Development Center, The Japan Wool Textile Co., Ltd.
    Kyoto University)

  • Shoji Uesugi

    (Medical Device Department, Nikke Medical Co., Ltd.)

  • Nynke A. Vepřek

    (New York University)

  • Florian Küllmer

    (Friedrich Schiller University Jena)

  • Veselin Nasufović

    (Friedrich Schiller University Jena)

  • Hironobu Uchiyama

    (Toray Research Center, Inc.)

  • Masaru Nakada

    (Toray Research Center, Inc.)

  • Yuji Otsuka

    (Toray Research Center, Inc.)

  • Yasuyuki Ito

    (Niigata University)

  • Vicente Herranz-Pérez

    (University of Valencia, CIBERNED)

  • José Manuel García-Verdugo

    (University of Valencia, CIBERNED)

  • Nobuhiko Ohno

    (Jichi Medical University, School of Medicine
    Division of Ultrastructural Research, National Institute for Physiological Sciences)

  • Hans-Dieter Arndt

    (Friedrich Schiller University Jena)

  • Dirk Trauner

    (New York University
    University of Pennsylvania)

  • Yasuhiko Tabata

    (Kyoto University)

  • Michihiro Igarashi

    (Niigata University)

  • Kazunobu Sawamoto

    (Nagoya City University Graduate School of Medical Sciences
    Division of Neural Development and Regeneration, National Institute for Physiological Sciences)

Abstract

Axonal growth cones mediate axonal guidance and growth regulation. We show that migrating neurons in mice possess a growth cone at the tip of their leading process, similar to that of axons, in terms of the cytoskeletal dynamics and functional responsivity through protein tyrosine phosphatase receptor type sigma (PTPσ). Migrating-neuron growth cones respond to chondroitin sulfate (CS) through PTPσ and collapse, which leads to inhibition of neuronal migration. In the presence of CS, the growth cones can revert to their extended morphology when their leading filopodia interact with heparan sulfate (HS), thus re-enabling neuronal migration. Implantation of an HS-containing biomaterial in the CS-rich injured cortex promotes the extension of the growth cone and improve the migration and regeneration of neurons, thereby enabling functional recovery. Thus, the growth cone of migrating neurons is responsive to extracellular environments and acts as a primary regulator of neuronal migration.

Suggested Citation

  • Chikako Nakajima & Masato Sawada & Erika Umeda & Yuma Takagi & Norihiko Nakashima & Kazuya Kuboyama & Naoko Kaneko & Satoaki Yamamoto & Haruno Nakamura & Naoki Shimada & Koichiro Nakamura & Kumiko Mat, 2024. "Identification of the growth cone as a probe and driver of neuronal migration in the injured brain," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45825-8
    DOI: 10.1038/s41467-024-45825-8
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    References listed on IDEAS

    as
    1. Xingqiao Xie & Ling Luo & Mingfu Liang & Wenchao Zhang & Ting Zhang & Cong Yu & Zhiyi Wei, 2020. "Structural basis of liprin-α-promoted LAR-RPTP clustering for modulation of phosphatase activity," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Bradley T. Lang & Jared M. Cregg & Marc A. DePaul & Amanda P. Tran & Kui Xu & Scott M. Dyck & Kathryn M. Madalena & Benjamin P. Brown & Yi-Lan Weng & Shuxin Li & Soheila Karimi-Abdolrezaee & Sarah A. , 2015. "Modulation of the proteoglycan receptor PTPσ promotes recovery after spinal cord injury," Nature, Nature, vol. 518(7539), pages 404-408, February.
    3. Shiaoching Gong & Chen Zheng & Martin L. Doughty & Kasia Losos & Nicholas Didkovsky & Uta B. Schambra & Norma J. Nowak & Alexandra Joyner & Gabrielle Leblanc & Mary E. Hatten & Nathaniel Heintz, 2003. "A gene expression atlas of the central nervous system based on bacterial artificial chromosomes," Nature, Nature, vol. 425(6961), pages 917-925, October.
    4. Roger A. Barker & Magdalena Götz & Malin Parmar, 2018. "New approaches for brain repair—from rescue to reprogramming," Nature, Nature, vol. 557(7705), pages 329-334, May.
    5. Ko Kobayakawa & Reiko Kobayakawa & Hideyuki Matsumoto & Yuichiro Oka & Takeshi Imai & Masahito Ikawa & Masaru Okabe & Toshio Ikeda & Shigeyoshi Itohara & Takefumi Kikusui & Kensaku Mori & Hitoshi Saka, 2007. "Innate versus learned odour processing in the mouse olfactory bulb," Nature, Nature, vol. 450(7169), pages 503-508, November.
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