{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T15:57:10Z","timestamp":1785859030629,"version":"3.56.0"},"reference-count":50,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2024,6,13]],"date-time":"2024-06-13T00:00:00Z","timestamp":1718236800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,6,13]],"date-time":"2024-06-13T00:00:00Z","timestamp":1718236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["17K07428"],"award-info":[{"award-number":["17K07428"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["19H04795"],"award-info":[{"award-number":["19H04795"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["20H03270"],"award-info":[{"award-number":["20H03270"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"MEXT | Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["16K07077"],"award-info":[{"award-number":["16K07077"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["JP21gm1310012"],"award-info":[{"award-number":["JP21gm1310012"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007449","name":"Takeda Science Foundation","doi-asserted-by":"publisher","award":["Y2018 research grant"],"award-info":[{"award-number":["Y2018 research grant"]}],"id":[{"id":"10.13039\/100007449","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007428","name":"Naito Foundation","doi-asserted-by":"publisher","award":["Y2018 research grant"],"award-info":[{"award-number":["Y2018 research grant"]}],"id":[{"id":"10.13039\/100007428","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100011746","name":"NOVARTIS Foundation (Japan) for the Promotion of Science (NOVARTIS Foundation","doi-asserted-by":"publisher","award":["FY2020 research grant"],"award-info":[{"award-number":["FY2020 research grant"]}],"id":[{"id":"10.13039\/501100011746","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004948","name":"Astellas Pharma","doi-asserted-by":"publisher","award":["FY2021 research grant"],"award-info":[{"award-number":["FY2021 research grant"]}],"id":[{"id":"10.13039\/501100004948","id-type":"DOI","asserted-by":"publisher"}]},{"name":"KOSE Cosmetology Research Foundation","award":["FY2021 research grant"],"award-info":[{"award-number":["FY2021 research grant"]}]},{"DOI":"10.13039\/501100004398","name":"Mitsubishi Foundation","doi-asserted-by":"publisher","award":["FY2021 research grant"],"award-info":[{"award-number":["FY2021 research grant"]}],"id":[{"id":"10.13039\/501100004398","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100031206","name":"Yamada Science Foundation","doi-asserted-by":"publisher","award":["FY2021 research grant"],"award-info":[{"award-number":["FY2021 research grant"]}],"id":[{"id":"10.13039\/100031206","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100012131","name":"Brain Science Foundation","doi-asserted-by":"crossref","award":["FY2021 research grant"],"award-info":[{"award-number":["FY2021 research grant"]}],"id":[{"id":"10.13039\/100012131","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EMBO Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The mammalian neocortex is formed by sequential radial migration of newborn excitatory neurons. Migrating neurons undergo a multipolar-to-bipolar transition at the subplate (SP) layer, where extracellular matrix (ECM) components are abundantly expressed. Here, we investigate the role of the ECM at the SP layer. We show that TGF-\u03b2 signaling-related ECM proteins, and their downstream effector, p-smad2\/3, are selectively expressed in the SP layer. We also find that migrating neurons express a disintegrin and metalloproteinase with thrombospondin motif 2 (ADAMTS2), an ECM metalloproteinase, just below the SP layer. Knockdown and knockout of Adamts2 suppresses the multipolar-to-bipolar transition of migrating neurons and disturbs radial migration. Time-lapse luminescence imaging of TGF-\u03b2 signaling indicates that ADAMTS2 activates this signaling pathway in migrating neurons during the multipolar-to-bipolar transition at the SP layer. Overexpression of TGF-\u03b22 in migrating neurons partially rescues migration defects in ADAMTS2 knockout mice. Our data suggest that ADAMTS2 secreted by the migrating multipolar neurons activates TGF-\u03b2 signaling by ECM remodeling of the SP layer, which might drive the multipolar to bipolar transition.<\/jats:p>","DOI":"10.1038\/s44319-024-00174-x","type":"journal-article","created":{"date-parts":[[2024,6,13]],"date-time":"2024-06-13T11:13:06Z","timestamp":1718277186000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["ADAMTS2 promotes radial migration by activating TGF-\u03b2 signaling in the developing neocortex"],"prefix":"10.1038","volume":"25","author":[{"given":"Noe","family":"Kaneko","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kumiko","family":"Hirai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minori","family":"Oshima","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0197-5478","authenticated-orcid":false,"given":"Kei","family":"Yura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0503-4969","authenticated-orcid":false,"given":"Mitsuharu","family":"Hattori","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nobuaki","family":"Maeda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0632-7341","authenticated-orcid":false,"given":"Chiaki","family":"Ohtaka-Maruyama","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,6,13]]},"reference":[{"key":"174_CR1","doi-asserted-by":"publisher","first-page":"5231","DOI":"10.1182\/blood-2012-07-442038","volume":"120","author":"A Arning","year":"2012","unstructured":"Arning A, Hiersche M, Witten A, Kurlemann G, Kurnik K, Manner D, Stoll M, Nowak-Gottl U (2012) A genome-wide association study identifies a gene network of ADAMTS genes in the predisposition to pediatric stroke. Blood 120:5231\u20135236","journal-title":"Blood"},{"key":"174_CR2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-17613-6","volume":"7","author":"K Asano","year":"2017","unstructured":"Asano K, Nelson CM, Nandadasa S, Aramaki-Hattori N, Lindner DJ, Alban T, Inagaki J, Ohtsuki T, Oohashi T, Apte SS et al (2017) Stromal versican regulates tumor growth by promoting angiogenesis. Sci Rep 7:17225","journal-title":"Sci Rep"},{"key":"174_CR3","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.matbio.2015.04.001","volume":"44-46","author":"M Bekhouche","year":"2015","unstructured":"Bekhouche M, Colige A (2015) The procollagen N-proteinases ADAMTS2, 3 and 14 in pathophysiology. Matrix Biol 44-46:46\u201353","journal-title":"Matrix Biol"},{"key":"174_CR4","doi-asserted-by":"publisher","first-page":"1741","DOI":"10.1096\/fj.15-279869","volume":"30","author":"M Bekhouche","year":"2016","unstructured":"Bekhouche M, Leduc C, Dupont L, Janssen L, Delolme F, Vadon-Le Goff S, Smargiasso N, Baiwir D, Mazzucchelli G, Zanella-Cleon I et al (2016) Determination of the substrate repertoire of ADAMTS2, 3, and 14 significantly broadens their functions and identifies extracellular matrix organization and TGF-beta signaling as primary targets. FASEB J 30:1741\u20131756","journal-title":"FASEB J"},{"key":"174_CR5","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1086\/302504","volume":"65","author":"A Colige","year":"1999","unstructured":"Colige A, Sieron AL, Li SW, Schwarze U, Petty E, Wertelecki W, Wilcox W, Krakow D, Cohn DH, Reardon W et al (1999) Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene. Am J Hum Genet 65:308\u2013317","journal-title":"Am J Hum Genet"},{"key":"174_CR6","doi-asserted-by":"publisher","first-page":"5756","DOI":"10.1074\/jbc.M105601200","volume":"277","author":"A Colige","year":"2002","unstructured":"Colige A, Vandenberghe I, Thiry M, Lambert CA, Van Beeumen J, Li SW, Prockop DJ, Lapiere CM, Nusgens BV (2002) Cloning and characterization of ADAMTS-14, a novel ADAMTS displaying high homology with ADAMTS-2 and ADAMTS-3. J Biol Chem 277:5756\u20135766","journal-title":"J Biol Chem"},{"key":"174_CR7","doi-asserted-by":"publisher","first-page":"1774","DOI":"10.1096\/fasebj.13.13.1774","volume":"13","author":"MR Duncan","year":"1999","unstructured":"Duncan MR, Frazier KS, Abramson S, Williams S, Klapper H, Huang X, Grotendorst GR (1999) Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by cAMP. FASEB J 13:1774\u20131786","journal-title":"FASEB J"},{"key":"174_CR8","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1016\/S0166-2236(00)01607-6","volume":"23","author":"JG Gleeson","year":"2000","unstructured":"Gleeson JG, Walsh CA (2000) Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 23:352\u2013359","journal-title":"Trends Neurosci"},{"key":"174_CR9","doi-asserted-by":"publisher","first-page":"990","DOI":"10.1016\/j.cell.2009.06.047","volume":"138","author":"S Guerrier","year":"2009","unstructured":"Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV, Chen K, Jin WL, Frost A, Polleux F (2009) The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138:990\u20131004","journal-title":"Cell"},{"key":"174_CR10","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.neuroscience.2018.10.021","volume":"396","author":"CL Han","year":"2019","unstructured":"Han CL, Zhao XM, Liu YP, Wang KL, Chen N, Hu W, Zhang JG, Ge M, Meng FG (2019) Gene expression profiling of two epilepsy models reveals the ECM\/integrin signaling pathway is involved in epiletogenesis. Neuroscience 396:187\u2013199","journal-title":"Neuroscience"},{"key":"174_CR11","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/S0306-4522(03)00100-3","volume":"119","author":"H Heuer","year":"2003","unstructured":"Heuer H, Christ S, Friedrichsen S, Brauer D, Winckler M, Bauer K, Raivich G (2003) Connective tissue growth factor: a novel marker of layer VII neurons in the rat cerebral cortex. Neuroscience 119:43\u201352","journal-title":"Neuroscience"},{"key":"174_CR12","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1038\/nrn3915","volume":"16","author":"A Hoerder-Suabedissen","year":"2015","unstructured":"Hoerder-Suabedissen A, Molnar Z (2015) Development, evolution and pathology of neocortical subplate neurons. Nat Rev Neurosci 16:133\u2013146","journal-title":"Nat Rev Neurosci"},{"key":"174_CR13","doi-asserted-by":"publisher","first-page":"1738","DOI":"10.1093\/cercor\/bhn195","volume":"19","author":"A Hoerder-Suabedissen","year":"2009","unstructured":"Hoerder-Suabedissen A, Wang WZ, Lee S, Davies KE, Goffinet AM, Rakic S, Parnavelas J, Reim K, Nicolic M, Paulsen O et al (2009) Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb Cortex 19:1738\u20131750","journal-title":"Cereb Cortex"},{"key":"174_CR14","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1186\/2045-3701-2-9","volume":"2","author":"F Huang","year":"2012","unstructured":"Huang F, Chen YG (2012) Regulation of TGF-beta receptor activity. Cell Biosci 2:9","journal-title":"Cell Biosci"},{"key":"174_CR15","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1091\/mbc.4.6.637","volume":"4","author":"A Igarashi","year":"1993","unstructured":"Igarashi A, Okochi H, Bradham DM, Grotendorst GR (1993) Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 4:637\u2013645","journal-title":"Mol Biol Cell"},{"key":"174_CR16","doi-asserted-by":"publisher","first-page":"32610","DOI":"10.1074\/jbc.M806331200","volume":"283","author":"M Ishii","year":"2008","unstructured":"Ishii M, Maeda N (2008) Oversulfated chondroitin sulfate plays critical roles in the neuronal migration in the cerebral cortex. J Biol Chem 283:32610\u201332620","journal-title":"J Biol Chem"},{"key":"174_CR17","doi-asserted-by":"publisher","first-page":"958","DOI":"10.1074\/jbc.270.2.958","volume":"270","author":"K Ito","year":"1995","unstructured":"Ito K, Shinomura T, Zako M, Ujita M, Kimata K (1995) Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J Biol Chem 270:958\u2013965","journal-title":"J Biol Chem"},{"key":"174_CR18","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1111\/age.12825","volume":"50","author":"JA Jaffey","year":"2019","unstructured":"Jaffey JA, Bullock G, Teplin E, Guo J, Villani NA, Mhlanga-Mutangadura T, Schnabel RD, Cohn LA, Johnson GS (2019) A homozygous ADAMTS2 nonsense mutation in a Doberman Pinscher dog with Ehlers Danlos syndrome and extreme skin fragility. Anim Genet 50:543\u2013545","journal-title":"Anim Genet"},{"key":"174_CR19","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1530\/JOE-10-0377","volume":"209","author":"SH Kim","year":"2011","unstructured":"Kim SH, Turnbull J, Guimond S (2011) Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 209:139\u2013151","journal-title":"J Endocrinol"},{"key":"174_CR20","doi-asserted-by":"publisher","first-page":"E5731","DOI":"10.1073\/pnas.1611532113","volume":"113","author":"Z Koledova","year":"2016","unstructured":"Koledova Z, Zhang X, Streuli C, Clarke RB, Klein OD, Werb Z, Lu P (2016) SPRY1 regulates mammary epithelial morphogenesis by modulating EGFR-dependent stromal paracrine signaling and ECM remodeling. Proc Natl Acad Sci USA 113:E5731\u20135740","journal-title":"Proc Natl Acad Sci USA"},{"key":"174_CR21","first-page":"61","volume":"8","author":"D Kothapalli","year":"1997","unstructured":"Kothapalli D, Frazier KS, Welply A, Segarini PR, Grotendorst GR (1997) Transforming growth factor beta induces anchorage-independent growth of NRK fibroblasts via a connective tissue growth factor-dependent signaling pathway. Cell Growth Differ 8:61\u201368","journal-title":"Cell Growth Differ"},{"key":"174_CR22","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1161\/01.ATV.19.7.1630","volume":"19","author":"JM Lemire","year":"1999","unstructured":"Lemire JM, Braun KR, Maurel P, Kaplan ED, Schwartz SM, Wight TN (1999) Versican\/PG-M isoforms in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19:1630\u20131639","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"174_CR23","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1042\/bj3550271","volume":"355","author":"SW Li","year":"2001","unstructured":"Li SW, Arita M, Fertala A, Bao Y, Kopen GC, Langsjo TK, Hyttinen MM, Helminen HJ, Prockop DJ (2001) Transgenic mice with inactive alleles for procollagen N-proteinase (ADAMTS-2) develop fragile skin and male sterility. Biochem J 355:271\u2013278","journal-title":"Biochem J"},{"key":"174_CR24","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.matbio.2022.01.005","volume":"107","author":"MP Lockhart-Cairns","year":"2022","unstructured":"Lockhart-Cairns MP, Cain SA, Dajani R, Steer R, Thomson J, Alanazi YF, Kielty CM, Baldock C (2022) Latent TGFbeta complexes are transglutaminase cross-linked to fibrillin to facilitate TGFbeta activation. Matrix Biol 107:24\u201339","journal-title":"Matrix Biol"},{"key":"174_CR25","doi-asserted-by":"publisher","first-page":"98","DOI":"10.3389\/fnins.2015.00098","volume":"9","author":"N Maeda","year":"2015","unstructured":"Maeda N (2015) Proteoglycans and neuronal migration in the cerebral cortex during development and disease. Front Neurosci 9:98","journal-title":"Front Neurosci"},{"key":"174_CR26","first-page":"273","volume":"3","author":"RK Margolis","year":"1996","unstructured":"Margolis RK, Rauch U, Maurel P, Margolis RU (1996) Neurocan and phosphacan: two major nervous tissue-specific chondroitin sulfate proteoglycans. Perspect Dev Neurobiol 3:273\u2013290","journal-title":"Perspect Dev Neurobiol"},{"key":"174_CR27","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1016\/j.devcel.2009.09.008","volume":"17","author":"DR McCulloch","year":"2009","unstructured":"McCulloch DR, Nelson CM, Dixon LJ, Silver DL, Wylie JD, Lindner V, Sasaki T, Cooley MA, Argraves WS, Apte SS (2009) ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression. Dev Cell 17:687\u2013698","journal-title":"Dev Cell"},{"key":"174_CR28","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1177\/002215540305100613","volume":"51","author":"OR Mook","year":"2003","unstructured":"Mook OR, Van Overbeek C, Ackema EG, Van Maldegem F, Frederiks WM (2003) In situ localization of gelatinolytic activity in the extracellular matrix of metastases of colon cancer in rat liver using quenched fluorogenic DQ-gelatin. J Histochem Cytochem 51:821\u2013829","journal-title":"J Histochem Cytochem"},{"key":"174_CR29","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1038\/83967","volume":"4","author":"B Nadarajah","year":"2001","unstructured":"Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143\u2013150","journal-title":"Nat Neurosci"},{"key":"174_CR30","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/j.matbio.2022.02.002","volume":"107","author":"S Neupane","year":"2022","unstructured":"Neupane S, Berardinelli SJ, Cameron DC, Grady RC, Komatsu DE, Percival CJ, Takeuchi M, Ito A, Liu TW, Nairn AV et al (2022) O-fucosylation of thrombospondin type 1 repeats is essential for ECM remodeling and signaling during bone development. Matrix Biol 107:77\u201396","journal-title":"Matrix Biol"},{"key":"174_CR31","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.1016\/j.neuroscience.2010.06.027","volume":"169","author":"K Nishimura","year":"2010","unstructured":"Nishimura K, Ishii M, Kuraoka M, Kamimura K, Maeda N (2010) Opposing functions of chondroitin sulfate and heparan sulfate during early neuronal polarization. Neuroscience 169:1535\u20131547","journal-title":"Neuroscience"},{"key":"174_CR32","doi-asserted-by":"publisher","first-page":"3181","DOI":"10.1523\/JNEUROSCI.3632-16.2017","volume":"37","author":"H Ogino","year":"2017","unstructured":"Ogino H, Hisanaga A, Kohno T, Kondo Y, Okumura K, Kamei T, Sato T, Asahara H, Tsuiji H, Fukata M et al (2017) Secreted metalloproteinase ADAMTS-3 inactivates reelin. J Neurosci 37:3181\u20133191","journal-title":"J Neurosci"},{"key":"174_CR33","doi-asserted-by":"publisher","first-page":"8","DOI":"10.3389\/fnana.2020.00008","volume":"14","author":"C Ohtaka-Maruyama","year":"2020","unstructured":"Ohtaka-Maruyama C (2020) Subplate neurons as an organizer of mammalian neocortical development. Front Neuroanat 14:8","journal-title":"Front Neuroanat"},{"key":"174_CR34","doi-asserted-by":"publisher","first-page":"1098","DOI":"10.1002\/cne.21350","volume":"502","author":"C Ohtaka-Maruyama","year":"2007","unstructured":"Ohtaka-Maruyama C, Miwa A, Kawano H, Kasai M, Okado H (2007) Spatial and temporal expression of RP58, a novel zinc finger transcriptional repressor, in mouse brain. J Comp Neurol 502:1098\u20131108","journal-title":"J Comp Neurol"},{"key":"174_CR35","doi-asserted-by":"publisher","first-page":"447","DOI":"10.3389\/fnins.2015.00447","volume":"9","author":"C Ohtaka-Maruyama","year":"2015","unstructured":"Ohtaka-Maruyama C, Okado H (2015) Molecular pathways underlying projection neuron production and migration during cerebral cortical development. Front Neurosci 9:447","journal-title":"Front Neurosci"},{"key":"174_CR36","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1126\/science.aar2866","volume":"360","author":"C Ohtaka-Maruyama","year":"2018","unstructured":"Ohtaka-Maruyama C, Okamoto M, Endo K, Oshima M, Kaneko N, Yura K, Okado H, Miyata T, Maeda N (2018) Synaptic transmission from subplate neurons controls radial migration of neocortical neurons. Science 360:313\u2013317","journal-title":"Science"},{"key":"174_CR37","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/0306-4522(94)90210-0","volume":"60","author":"A Oohira","year":"1994","unstructured":"Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda N (1994) Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 60:145\u2013157","journal-title":"Neuroscience"},{"key":"174_CR38","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1002\/dvdy.10282","volume":"227","author":"S Popp","year":"2003","unstructured":"Popp S, Andersen JS, Maurel P, Margolis RU (2003) Localization of aggrecan and versican in the developing rat central nervous system. Dev Dyn 227:143\u2013149","journal-title":"Dev Dyn"},{"key":"174_CR39","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1126\/science.183.4123.425","volume":"183","author":"P Rakic","year":"1974","unstructured":"Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425\u2013427","journal-title":"Science"},{"key":"174_CR40","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1002\/dvdy.331","volume":"251","author":"D Rifkin","year":"2022","unstructured":"Rifkin D, Sachan N, Singh K, Sauber E, Tellides G, Ramirez F (2022) The role of LTBPs in TGF beta signaling. Dev Dyn 251:95\u2013104","journal-title":"Dev Dyn"},{"key":"174_CR41","doi-asserted-by":"publisher","first-page":"a003228","DOI":"10.1101\/cshperspect.a003228","volume":"3","author":"P Schedin","year":"2011","unstructured":"Schedin P, Keely PJ (2011) Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb Perspect Biol 3:a003228","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"174_CR42","doi-asserted-by":"publisher","first-page":"62","DOI":"10.3389\/fncel.2015.00062","volume":"9","author":"S Singh","year":"2015","unstructured":"Singh S, Solecki DJ (2015) Polarity transitions during neurogenesis and germinal zone exit in the developing central nervous system. Front Cell Neurosci 9:62","journal-title":"Front Cell Neurosci"},{"key":"174_CR43","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1016\/j.neuroscience.2013.08.050","volume":"253","author":"S Soleman","year":"2013","unstructured":"Soleman S, Filippov MA, Dityatev A, Fawcett JW (2013) Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253:194\u2013213","journal-title":"Neuroscience"},{"key":"174_CR44","doi-asserted-by":"publisher","first-page":"50","DOI":"10.3389\/fpsyt.2012.00050","volume":"3","author":"H Stolp","year":"2012","unstructured":"Stolp H, Neuhaus A, Sundramoorthi R, Molnar Z (2012) The long and the short of it: gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front Psychiatry 3:50","journal-title":"Front Psychiatry"},{"key":"174_CR45","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1007\/s00795-015-0127-y","volume":"49","author":"H Tabata","year":"2016","unstructured":"Tabata H, Nagata K (2016) Decoding the molecular mechanisms of neuronal migration using in utero electroporation. Med Mol Morphol 49:63\u201375","journal-title":"Med Mol Morphol"},{"key":"174_CR46","doi-asserted-by":"publisher","first-page":"9996","DOI":"10.1523\/JNEUROSCI.23-31-09996.2003","volume":"23","author":"H Tabata","year":"2003","unstructured":"Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996\u201310001","journal-title":"J Neurosci"},{"key":"174_CR47","doi-asserted-by":"publisher","first-page":"2501","DOI":"10.1016\/j.yexcr.2008.05.018","volume":"314","author":"O Tatti","year":"2008","unstructured":"Tatti O, Vehvilainen P, Lehti K, Keski-Oja J (2008) MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp Cell Res 314:2501\u20132514","journal-title":"Exp Cell Res"},{"key":"174_CR48","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1038\/sj.cr.7290318","volume":"15","author":"YJ Wu","year":"2005","unstructured":"Wu YJ, La Pierre DP, Wu J, Yee AJ, Yang BB (2005) The interaction of versican with its binding partners. Cell Res 15:483\u2013494","journal-title":"Cell Res"},{"key":"174_CR49","doi-asserted-by":"publisher","DOI":"10.1016\/j.mcn.2019.103401","volume":"100","author":"Y Yamakage","year":"2019","unstructured":"Yamakage Y, Kato M, Hongo A, Ogino H, Ishii K, Ishizuka T, Kamei T, Tsuiji H, Miyamoto T, Oishi H et al (2019) A disintegrin and metalloproteinase with thrombospondin motifs 2 cleaves and inactivates Reelin in the postnatal cerebral cortex and hippocampus, but not in the cerebellum. Mol Cell Neurosci 100:103401","journal-title":"Mol Cell Neurosci"},{"key":"174_CR50","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.cell.2010.06.010","volume":"142","author":"JJ Yi","year":"2010","unstructured":"Yi JJ, Barnes AP, Hand R, Polleux F, Ehlers MD (2010) TGF-beta signaling specifies axons during brain development. Cell 142:144\u2013157","journal-title":"Cell"}],"container-title":["EMBO Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/s44319-024-00174-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1038\/s44319-024-00174-x","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1038\/s44319-024-00174-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T15:03:19Z","timestamp":1785855799000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1038\/s44319-024-00174-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,13]]},"references-count":50,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7,11]]}},"alternative-id":["174"],"URL":"https:\/\/doi.org\/10.1038\/s44319-024-00174-x","relation":{},"ISSN":["1469-3178"],"issn-type":[{"value":"1469-3178","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,13]]},"assertion":[{"value":"19 August 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 May 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 June 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 June 2024","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Disclosure and competing interests statement"}}],"article-number":"16"}}