PMID- 38512724 OWN - NLM STAT- MEDLINE DCOM- 20240325 LR - 20240325 IS - 2050-084X (Electronic) IS - 2050-084X (Linking) VI - 12 DP - 2024 Mar 21 TI - Assembly of neuron- and radial glial-cell-derived extracellular matrix molecules promotes radial migration of developing cortical neurons. LID - 10.7554/eLife.92342 [doi] LID - RP92342 AB - 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. CI - (c) 2023, Mubuchi et al. FAU - Mubuchi, Ayumu AU - Mubuchi A AD - Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan. FAU - Takechi, Mina AU - Takechi M AD - Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan. FAU - Nishio, Shunsuke AU - Nishio S AUID- ORCID: 0000-0003-3420-2578 AD - Faculty of Food and Agricultural Sciences, Fukushima University, Fukushima, Japan. FAU - Matsuda, Tsukasa AU - Matsuda T AD - Faculty of Food and Agricultural Sciences, Fukushima University, Fukushima, Japan. FAU - Itoh, Yoshifumi AU - Itoh Y AUID- ORCID: 0000-0002-2128-2823 AD - Kennedy Institute of Rheumatology, University of Oxford, Oxford, United Kingdom. FAU - Sato, Chihiro AU - Sato C AD - Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan. AD - Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan. AD - Institute for Glyco-core Research, Nagoya University, Nagoya, Japan. FAU - Kitajima, Ken AU - Kitajima K AD - Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan. AD - Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan. AD - Institute for Glyco-core Research, Nagoya University, Nagoya, Japan. FAU - Kitagawa, Hiroshi AU - Kitagawa H AUID- ORCID: 0000-0002-9307-7079 AD - Laboratory of Biochemistry, Kobe Pharmaceutical University, Kobe, Japan. FAU - Miyata, Shinji AU - Miyata S AUID- ORCID: 0000-0001-6635-1645 AD - Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan. LA - eng GR - 15K21067/Ministry of Education, Culture, Sports, Science and Technology/ GR - 18K06130/Ministry of Education, Culture, Sports, Science and Technology/ GR - 21H05681/Ministry of Education, Culture, Sports, Science and Technology/ GR - Lotte Shigemitsu Prize/Lotte Foundation/ PT - Journal Article DEP - 20240321 PL - England TA - Elife JT - eLife JID - 101579614 RN - 0 (Chondroitin Sulfate Proteoglycans) SB - IM UOF - doi: 10.1101/2022.09.03.506497 UOF - doi: 10.7554/eLife.92342.1 UOF - doi: 10.7554/eLife.92342.2 MH - Animals MH - Mice MH - *Neurons/physiology MH - *Extracellular Matrix/metabolism MH - Cerebral Cortex/metabolism MH - Cell Movement/physiology MH - Chondroitin Sulfate Proteoglycans/metabolism PMC - PMC10957175 OTO - NOTNLM OT - biochemistry OT - chemical biology OT - cortical development OT - extracellular matrix OT - hyaluronic acid OT - mouse OT - neuroscience OT - proteoglycans OT - radial migration OT - tenascin COIS- AM, MT, SN, TM, YI, CS, KK, HK, SM No competing interests declared EDAT- 2024/03/21 18:45 MHDA- 2024/03/25 06:42 PMCR- 2024/03/21 CRDT- 2024/03/21 12:53 PHST- 2024/03/25 06:42 [medline] PHST- 2024/03/21 18:45 [pubmed] PHST- 2024/03/21 12:53 [entrez] PHST- 2024/03/21 00:00 [pmc-release] AID - 92342 [pii] AID - 10.7554/eLife.92342 [doi] PST - epublish SO - Elife. 2024 Mar 21;12:RP92342. doi: 10.7554/eLife.92342.