IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45825-8.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45825-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45825-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Myung Chung & Katsutoshi Imanaka & Ziyan Huang & Akiyuki Watarai & Mu-Yun Wang & Kentaro Tao & Hirotaka Ejima & Tomomi Aida & Guoping Feng & Teruhiro Okuyama, 2024. "Conditional knockout of Shank3 in the ventral CA1 by quantitative in vivo genome-editing impairs social memory in mice," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Masahiro Mitsuhashi & Reona Yamaguchi & Toshinari Kawasaki & Satoko Ueno & Yiping Sun & Kaoru Isa & Jun Takahashi & Kenta Kobayashi & Hirotaka Onoe & Ryosuke Takahashi & Tadashi Isa, 2024. "Stage-dependent role of interhemispheric pathway for motor recovery in primates," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Brandon W. Hughes & Jessica L. Huebschman & Evgeny Tsvetkov & Benjamin M. Siemsen & Kirsten K. Snyder & Rose Marie Akiki & Daniel J. Wood & Rachel D. Penrod & Michael D. Scofield & Stefano Berto & Mak, 2024. "NPAS4 supports cocaine-conditioned cues in rodents by controlling the cell type-specific activation balance in the nucleus accumbens," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Clara Morral & Arshad Ayyaz & Hsuan-Cheng Kuo & Mardi Fink & Ioannis I. Verginadis & Andrea R. Daniel & Danielle N. Burner & Lucy M. Driver & Sloane Satow & Stephanie Hasapis & Reem Ghinnagow & Lixia , 2024. "p53 promotes revival stem cells in the regenerating intestine after severe radiation injury," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Sofia Madsen & Ana C. Delgado & Christelle Cadilhac & Vanille Maillard & Fabrice Battiston & Carla Marie Igelbüscher & Simon De Neck & Elia Magrinelli & Denis Jabaudon & Ludovic Telley & Fiona Doetsch, 2024. "A fluorescent perilipin 2 knock-in mouse model reveals a high abundance of lipid droplets in the developing and adult brain," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Yun-Feng Zhang & Jialiang Wu & Yingqi Wang & Natalie L. Johnson & Janardhan P. Bhattarai & Guanqing Li & Wenqiang Wang & Camilo Guevara & Hannah Shoenhard & Marc V. Fuccillo & Daniel W. Wesson & Mingh, 2023. "Ventral striatal islands of Calleja neurons bidirectionally mediate depression-like behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Paul B Manis & Michael R Kasten & Ruili Xie, 2019. "Classification of neurons in the adult mouse cochlear nucleus: Linear discriminant analysis," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-14, October.
    8. Gwen-Jirō Clochard & Aby Mbengue & Clément Mettling & Birane Diouf & Charlotte Faurie & Omar Sene & Emilie Chancerel & Erwan Guichoux & Guillaume Hollard & Michel Raymond & Marc Willinger, 2023. "The effect of the 7R allele at the DRD4 locus on risk tolerance is independent of background risk in Senegalese fishermen," Post-Print hal-03954770, HAL.
    9. Jong Hoon Won & Jacob S. Choi & Joon-Il Jun, 2022. "CCN1 interacts with integrins to regulate intestinal stem cell proliferation and differentiation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Fan Mei & Chen Zhao & Shangjin Li & Zeping Xue & Yueyang Zhao & Yihua Xu & Rongrong Ye & He You & Peng Yu & Xinyu Han & Gregory V. Carr & Daniel R. Weinberger & Feng Yang & Bai Lu, 2024. "Ngfr+ cholinergic projection from SI/nBM to mPFC selectively regulates temporal order recognition memory," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Josephine A. Mapunda & Javier Pareja & Mykhailo Vladymyrov & Elisa Bouillet & Pauline Hélie & Petr Pleskač & Sara Barcos & Johanna Andrae & Dietmar Vestweber & Donald M. McDonald & Christer Betsholtz , 2023. "VE-cadherin in arachnoid and pia mater cells serves as a suitable landmark for in vivo imaging of CNS immune surveillance and inflammation," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    12. Chang Li & Natalie B. Saliba & Hannah Martin & Nicole A. Losurdo & Kian Kolahdouzan & Riyan Siddiqui & Destynie Medeiros & Wei Li, 2023. "Purkinje cell dopaminergic inputs to astrocytes regulate cerebellar-dependent behavior," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Solomiia Korchynska & Patrick Rebernik & Marko Pende & Laura Boi & Alán Alpár & Ramon Tasan & Klaus Becker & Kira Balueva & Saiedeh Saghafi & Peer Wulff & Tamas L. Horvath & Gilberto Fisone & Hans-Ulr, 2022. "A hypothalamic dopamine locus for psychostimulant-induced hyperlocomotion in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    14. Mehmet Can Uçar & Edouard Hannezo & Emmi Tiilikainen & Inam Liaqat & Emma Jakobsson & Harri Nurmi & Kari Vaahtomeri, 2023. "Self-organized and directed branching results in optimal coverage in developing dermal lymphatic networks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    15. Kevin W. Zhu & Shawn D. Burton & Maira H. Nagai & Justin D. Silverman & Claire A. March & Matt Wachowiak & Hiroaki Matsunami, 2022. "Decoding the olfactory map through targeted transcriptomics links murine olfactory receptors to glomeruli," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Isaac Francos-Quijorna & Marina Sánchez-Petidier & Emily R. Burnside & Smaranda R. Badea & Abel Torres-Espin & Lucy Marshall & Fred Winter & Joost Verhaagen & Victoria Moreno-Manzano & Elizabeth J. Br, 2022. "Chondroitin sulfate proteoglycans prevent immune cell phenotypic conversion and inflammation resolution via TLR4 in rodent models of spinal cord injury," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    17. Matthieu Maroteaux & Emmanuel Valjent & Sophie Longueville & Piotr Topilko & Jean-Antoine Girault & Denis Hervé, 2014. "Role of the Plasticity-Associated Transcription Factor Zif268 in the Early Phase of Instrumental Learning," PLOS ONE, Public Library of Science, vol. 9(1), pages 1-13, January.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45825-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.