Nature Communications (Mar 2024)
Identification of the growth cone as a probe and driver of neuronal migration in the injured brain
- Chikako Nakajima,
- Masato Sawada,
- Erika Umeda,
- Yuma Takagi,
- Norihiko Nakashima,
- Kazuya Kuboyama,
- Naoko Kaneko,
- Satoaki Yamamoto,
- Haruno Nakamura,
- Naoki Shimada,
- Koichiro Nakamura,
- Kumiko Matsuno,
- Shoji Uesugi,
- Nynke A. Vepřek,
- Florian Küllmer,
- Veselin Nasufović,
- Hironobu Uchiyama,
- Masaru Nakada,
- Yuji Otsuka,
- Yasuyuki Ito,
- Vicente Herranz-Pérez,
- José Manuel García-Verdugo,
- Nobuhiko Ohno,
- Hans-Dieter Arndt,
- Dirk Trauner,
- Yasuhiko Tabata,
- Michihiro Igarashi,
- Kazunobu Sawamoto
Affiliations
- Chikako Nakajima
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Masato Sawada
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Erika Umeda
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Yuma Takagi
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Norihiko Nakashima
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Kazuya Kuboyama
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Naoko Kaneko
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Satoaki Yamamoto
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- Haruno Nakamura
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, 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.
- Shoji Uesugi
- Medical Device Department, Nikke Medical Co., Ltd.
- Nynke A. Vepřek
- Department of Chemistry, New York University
- Florian Küllmer
- Institute for Organic Chemistry and Macromolecular Chemistry, Friedrich Schiller University Jena
- Veselin Nasufović
- Institute for Organic Chemistry and Macromolecular Chemistry, Friedrich Schiller University Jena
- Hironobu Uchiyama
- Toray Research Center, Inc.
- Masaru Nakada
- Toray Research Center, Inc.
- Yuji Otsuka
- Toray Research Center, Inc.
- Yasuyuki Ito
- Department of Neurochemistry and Molecular Cell Biology, School of Medicine and Graduate School of Medical/Dental Sciences, Niigata University
- Vicente Herranz-Pérez
- Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia, CIBERNED
- José Manuel García-Verdugo
- Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia, CIBERNED
- Nobuhiko Ohno
- Department of Anatomy, Division of Histology and Cell Biology, Jichi Medical University, School of Medicine
- Hans-Dieter Arndt
- Institute for Organic Chemistry and Macromolecular Chemistry, Friedrich Schiller University Jena
- Dirk Trauner
- Department of Chemistry, New York University
- Yasuhiko Tabata
- Laboratory of Biomaterials, Department of Regeneration Science and Engineering, Institute for Life and Medical Sciences (LiMe), Kyoto University
- Michihiro Igarashi
- Department of Neurochemistry and Molecular Cell Biology, School of Medicine and Graduate School of Medical/Dental Sciences, Niigata University
- Kazunobu Sawamoto
- Department of Developmental and Regenerative Neurobiology, Institute of Brain Science, Nagoya City University Graduate School of Medical Sciences
- DOI
- https://doi.org/10.1038/s41467-024-45825-8
- Journal volume & issue
-
Vol. 15,
no. 1
pp. 1 – 19
Abstract
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.
