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

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 recept...

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Published in:	Nature communications Vol. 15; no. 1; pp. 1877 - 19
Main Authors:	Nakajima, Chikako, Sawada, Masato, Umeda, Erika, Takagi, Yuma, Nakashima, Norihiko, Kuboyama, Kazuya, Kaneko, Naoko, Yamamoto, Satoaki, Nakamura, Haruno, Shimada, Naoki, Nakamura, Koichiro, Matsuno, Kumiko, Uesugi, Shoji, Vepřek, Nynke A., Küllmer, Florian, Nasufović, Veselin, Uchiyama, Hironobu, Nakada, Masaru, Otsuka, Yuji, Ito, Yasuyuki, Herranz-Pérez, Vicente, García-Verdugo, José Manuel, Ohno, Nobuhiko, Arndt, Hans-Dieter, Trauner, Dirk, Tabata, Yasuhiko, Igarashi, Michihiro, Sawamoto, Kazunobu
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 09-03-2024 Nature Publishing Group Nature Portfolio
Subjects:	13/106 13/107 13/51 14 14/19 14/28 14/63 59 631/378/87 64 64/60 692/617/375/1345/3195 Animals Axon guidance Axonogenesis Axons Axons - metabolism Biomaterials Biomedical materials Brain Brain - metabolism Cell migration Cells, Cultured Chondroitin sulfate Chondroitin Sulfates - metabolism Cones Cytoskeleton Extracellular matrix Filopodia Growth cones Growth Cones - metabolism Heparan sulfate Humanities and Social Sciences Injuries Mice multidisciplinary Neurogenesis Neurons Protein-tyrosine-phosphatase Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics Receptor-Like Protein Tyrosine Phosphatases, Class 2 - metabolism Recovery Recovery of function Regeneration Science Science (multidisciplinary) Sulfates Surgical implants Tyrosine
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Summary:	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. Structure and functions of the tip of migratory neurons remain elusive. Here, the authors show that the PTPσ-expressing growth cone senses extracellular matrix changes and drives neuronal migration in the injured brain, leading to the functional recovery.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	2041-1723 2041-1723
DOI:	10.1038/s41467-024-45825-8