Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons
Radial neuronal migration is a key neurodevelopmental event for proper cortical laminar organization. The multipolar-to-bipolar transition, a critical step in establishing neuronal polarity during radial migration, occurs in the subplate/intermediate zone (SP/IZ), a distinct region of the embryonic...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/92342 |
| _version_ | 1797253648983523328 |
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| author | Ayumu Mubuchi Mina Takechi Shunsuke Nishio Tsukasa Matsuda Yoshifumi Itoh Chihiro Sato Ken Kitajima Hiroshi Kitagawa Shinji Miyata |
| author_facet | Ayumu Mubuchi Mina Takechi Shunsuke Nishio Tsukasa Matsuda Yoshifumi Itoh Chihiro Sato Ken Kitajima Hiroshi Kitagawa Shinji Miyata |
| author_sort | Ayumu Mubuchi |
| collection | DOAJ |
| description | Radial neuronal migration is a key neurodevelopmental event for proper cortical laminar organization. The multipolar-to-bipolar transition, a critical step in establishing neuronal polarity during radial migration, occurs in the subplate/intermediate zone (SP/IZ), a distinct region of the embryonic cerebral cortex. It has been known that the extracellular matrix (ECM) molecules are enriched in the SP/IZ. However, the molecular constitution and functions of the ECM formed in this region remain poorly understood. Here, we identified neurocan (NCAN) as a major chondroitin sulfate proteoglycan in the mouse SP/IZ. NCAN binds to both radial glial-cell-derived tenascin-C (TNC) and hyaluronan (HA), a large linear polysaccharide, forming a ternary complex of NCAN, TNC, and HA in the SP/IZ. Developing cortical neurons make contact with the ternary complex during migration. The enzymatic or genetic disruption of the ternary complex impairs radial migration by suppressing the multipolar-to-bipolar transition. Furthermore, both TNC and NCAN promoted the morphological maturation of cortical neurons in vitro. The present results provide evidence for the cooperative role of neuron- and radial glial-cell-derived ECM molecules in cortical development. |
| first_indexed | 2024-04-24T21:37:25Z |
| format | Article |
| id | doaj.art-6a99df04125f444283a95d9bcb4a49cf |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-24T21:37:25Z |
| publishDate | 2024-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-6a99df04125f444283a95d9bcb4a49cf2024-03-21T16:37:07ZengeLife Sciences Publications LtdeLife2050-084X2024-03-011210.7554/eLife.92342Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neuronsAyumu Mubuchi0Mina Takechi1Shunsuke Nishio2https://orcid.org/0000-0003-3420-2578Tsukasa Matsuda3Yoshifumi Itoh4https://orcid.org/0000-0002-2128-2823Chihiro Sato5Ken Kitajima6Hiroshi Kitagawa7https://orcid.org/0000-0002-9307-7079Shinji Miyata8https://orcid.org/0000-0001-6635-1645Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, JapanGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, JapanFaculty of Food and Agricultural Sciences, Fukushima University, Fukushima, JapanFaculty of Food and Agricultural Sciences, Fukushima University, Fukushima, JapanKennedy Institute of Rheumatology, University of Oxford, Oxford, United KingdomGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan; Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan; Institute for Glyco-core Research, Nagoya University, Nagoya, JapanGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan; Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan; Institute for Glyco-core Research, Nagoya University, Nagoya, JapanLaboratory of Biochemistry, Kobe Pharmaceutical University, Kobe, JapanGraduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, JapanRadial neuronal migration is a key neurodevelopmental event for proper cortical laminar organization. The multipolar-to-bipolar transition, a critical step in establishing neuronal polarity during radial migration, occurs in the subplate/intermediate zone (SP/IZ), a distinct region of the embryonic cerebral cortex. It has been known that the extracellular matrix (ECM) molecules are enriched in the SP/IZ. However, the molecular constitution and functions of the ECM formed in this region remain poorly understood. Here, we identified neurocan (NCAN) as a major chondroitin sulfate proteoglycan in the mouse SP/IZ. NCAN binds to both radial glial-cell-derived tenascin-C (TNC) and hyaluronan (HA), a large linear polysaccharide, forming a ternary complex of NCAN, TNC, and HA in the SP/IZ. Developing cortical neurons make contact with the ternary complex during migration. The enzymatic or genetic disruption of the ternary complex impairs radial migration by suppressing the multipolar-to-bipolar transition. Furthermore, both TNC and NCAN promoted the morphological maturation of cortical neurons in vitro. The present results provide evidence for the cooperative role of neuron- and radial glial-cell-derived ECM molecules in cortical development.https://elifesciences.org/articles/92342extracellular matrixproteoglycanscortical developmentradial migrationhyaluronic acidtenascin |
| spellingShingle | Ayumu Mubuchi Mina Takechi Shunsuke Nishio Tsukasa Matsuda Yoshifumi Itoh Chihiro Sato Ken Kitajima Hiroshi Kitagawa Shinji Miyata Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons eLife extracellular matrix proteoglycans cortical development radial migration hyaluronic acid tenascin |
| title | Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| title_full | Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| title_fullStr | Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| title_full_unstemmed | Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| title_short | Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| title_sort | assembly of neuron and radial glial cell derived extracellular matrix molecules promotes radial migration of developing cortical neurons |
| topic | extracellular matrix proteoglycans cortical development radial migration hyaluronic acid tenascin |
| url | https://elifesciences.org/articles/92342 |
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