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 and Kazunobu Sawamoto ()
Additional contact information
Chikako Nakajima: Nagoya City University Graduate School of Medical Sciences
Masato Sawada: Nagoya City University Graduate School of Medical 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
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.
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
Hans-Dieter Arndt: Friedrich Schiller University Jena
Dirk Trauner: New York University
Yasuhiko Tabata: Kyoto University
Michihiro Igarashi: Niigata University
Kazunobu Sawamoto: Nagoya City University Graduate School of Medical Sciences

Nature Communications, 2024, vol. 15, issue 1, 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.

Date: 2024
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DOI: 10.1038/s41467-024-45825-8

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