{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T10:27:02Z","timestamp":1787567222408,"version":"build-2736575974"},"reference-count":79,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T00:00:00Z","timestamp":1783555200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T00:00:00Z","timestamp":1783555200000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T00:00:00Z","timestamp":1783555200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"CIHR Canada Research Chair"},{"id":[{"id":"https:\/\/ror.org\/01gavpb45","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100020986","name":"Jewish General Hospital Foundation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100020986","id-type":"DOI","asserted-by":"crossref"}]},{"id":[{"id":"https:\/\/ror.org\/056jjra10","id-type":"ROR","asserted-by":"publisher"}]},{"name":"CIHR Project Grant","award":["PJT-189995"],"award-info":[{"award-number":["PJT-189995"]}]},{"award":["PJT-189995"],"award-info":[{"award-number":["PJT-189995"]}],"id":[{"id":"https:\/\/ror.org\/01gavpb45","id-type":"ROR","asserted-by":"publisher"}]},{"name":"NSERC Discovery Grant","award":["RGPIN-2024-05603"],"award-info":[{"award-number":["RGPIN-2024-05603"]}]},{"award":["RGPIN-2024-05603"],"award-info":[{"award-number":["RGPIN-2024-05603"]}],"id":[{"id":"https:\/\/ror.org\/01h531d29","id-type":"ROR","asserted-by":"publisher"}]},{"name":"CIHR Funds"},{"id":[{"id":"https:\/\/ror.org\/01gavpb45","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>\n                    The cerebral cortex is a multi-layered structure generated through the migration of neural precursors from their birthplace in the ventricular zone to their destination within the cortical plate. Neuronal migration defects are responsible for many human pathologies collectively called neuronal migration disorders, which include subcortical band heterotopia and cobblestone brain (COB) malformation. One example of a protein involved in a neuronal migration disorder is the echinoderm microtubule-associated protein-like 1 (EML1) protein, one of six members of the mammalian EML family. Absence of EML1 protein results in subcortical band heterotopia in mice and humans. Here, we report that the absence of the paralogous protein EML3 leads to delayed embryonic development and small size, and a COB-like phenotype with neuronal ectopias in the dorsal telencephalon. We found that EML3 is expressed in the neuroepithelium and meningeal mesenchyme when those tissues participate in pial basement membrane (PBM) formation. Transmission electron microscopy demonstrated that the extracellular matrix of the PBM is structurally abnormal in\n                    <jats:italic>Eml3<\/jats:italic>\n                    null mice when the first radially migrating neurons arrive. The reduced structural integrity of the PBM leads to focal over-migration of neurons into the subarachnoid space. These findings strengthen the link between the EML protein family and cortical neuronal migration defects by identifying\n                    <jats:italic>Eml3<\/jats:italic>\n                    as the first EML family member whose absence leads to over-migration of neuroblasts. Moreover, we report the first COB-like phenotype with PBM structural defects when a single microtubule-associated protein is deleted.\n                  <\/jats:p>","DOI":"10.7554\/elife.107102","type":"journal-article","created":{"date-parts":[[2025,7,24]],"date-time":"2025-07-24T14:30:45Z","timestamp":1753367445000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.107102","source":"Crossref","is-referenced-by-count":0,"title":["The microtubule-binding protein EML3 is required for mammalian embryonic growth and cerebral cortical development, and Eml3 null mice are a model of cobblestone brain malformation"],"prefix":"10.7554","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0009-0003-6275-0173","authenticated-orcid":true,"given":"Isabelle","family":"Carrier","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Lady Davis Research Institute for Medical Research of the Montreal Jewish General Hospital, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"corresponding-author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-5064-8256","authenticated-orcid":true,"given":"Eduardo","family":"Diez","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Lady Davis Research Institute for Medical Research of the Montreal Jewish General Hospital, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"corresponding-author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Valerio E","family":"Piscopo","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Lady Davis Research Institute for Medical Research of the Montreal Jewish General Hospital, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Montreal Neurological Institute-Hospital, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4706-9975","authenticated-orcid":true,"given":"Susanne","family":"Bechstedt","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Anatomy and Cell Biology, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Centre de recherche en biologie structurale, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Hans","family":"van Bokhoven","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05wg1m734","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Human Genetics, Radboud University Medical Center, Donders Institute for Brain, Cognition, and Behaviour","place":["Nijmegen, Netherlands"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"resources","vocabulary":"credit"}]},{"given":"Myriam","family":"Srour","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04wc5jk96","id-type":"ROR","asserted-by":"publisher"}],"name":"Montreal Children\u2019s Hospital, MUHC-RI","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Pediatrics, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Neurology and Neurosurgery, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"resources","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2663-025X","authenticated-orcid":true,"given":"Albert M","family":"Berghuis","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Centre de recherche en biologie structurale, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biochemistry, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Microbiology and Immunology, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"methodology","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"given":"Stefano","family":"Stifani","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Montreal Neurological Institute-Hospital, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Neurology and Neurosurgery, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1483-8691","authenticated-orcid":true,"given":"Yojiro","family":"Yamanaka","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Goodman Cancer Institute, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Human Genetics, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Roderick","family":"McInnes","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Lady Davis Research Institute for Medical Research of the Montreal Jewish General Hospital, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biochemistry, McGill University","place":["Montr\u00e9al, Canada"]},{"id":[{"id":"https:\/\/ror.org\/01pxwe438","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Human Genetics, McGill University","place":["Montr\u00e9al, Canada"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]}],"member":"4374","published-online":{"date-parts":[[2026,7,9]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","DOI":"10.1126\/scisignal.aaw2939","type":"journal-article","article-title":"Mitotic phosphorylation by NEK6 and NEK7 reduces the microtubule affinity of EML4 to promote chromosome congression","volume":"12","author":"Adib","year":"2019","journal-title":"Science Signaling"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"17154","DOI":"10.1074\/jbc.R115.638452","type":"journal-article","article-title":"Building the microtubule cytoskeleton piece by piece","volume":"290","author":"Alfaro-Aco","year":"2015","journal-title":"The Journal of Biological Chemistry"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1016\/s0896-6273(04)00140-0","type":"journal-article","article-title":"Radial glia serve as neuronal progenitors in all regions of the central nervous system","volume":"41","author":"Anthony","year":"2004","journal-title":"Neuron"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.neuron.2004.12.036","type":"journal-article","article-title":"Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo","volume":"45","author":"Arlotta","year":"2005","journal-title":"Neuron"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"1348","DOI":"10.1093\/brain\/aws019","type":"journal-article","article-title":"A developmental and genetic classification for malformations of cortical development: update 2012","volume":"135","author":"Barkovich","year":"2012","journal-title":"Brain"},{"key":"bib6","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a022392","type":"journal-article","article-title":"Malformations of cortical development and epilepsy","volume":"5","author":"Barkovich","year":"2015","journal-title":"Cold Spring Harbor Perspectives in Medicine"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"1536","DOI":"10.1093\/cercor\/bhm184","type":"journal-article","article-title":"A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone","volume":"18","author":"Bayatti","year":"2008","journal-title":"Cerebral Cortex"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"13129","DOI":"10.1073\/pnas.1002285107","type":"journal-article","article-title":"Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex","volume":"107","author":"Bedogni","year":"2010","journal-title":"PNAS"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1086\/342975","type":"journal-article","article-title":"Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome","volume":"71","author":"Beltr\u00e1n-Valero de Bernab\u00e9","year":"2002","journal-title":"American Journal of Human Genetics"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"7551","DOI":"10.1523\/JNEUROSCI.6716-10.2011","type":"journal-article","article-title":"Abnormal neuronal migration changes the fate of developing neurons in the postnatal olfactory bulb","volume":"31","author":"Belvindrah","year":"2011","journal-title":"The Journal of Neuroscience"},{"key":"bib11","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-15253-4","type":"journal-article","article-title":"Eml1 loss impairs apical progenitor spindle length and soma shape in the developing cerebral cortex","volume":"7","author":"Bizzotto","year":"2017","journal-title":"Scientific Reports"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1016\/j.tcb.2019.07.004","type":"journal-article","article-title":"Microtubule-associated proteins: structuring the cytoskeleton","volume":"29","author":"Bodakuntla","year":"2019","journal-title":"Trends in Cell Biology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1038\/nrm3904","type":"journal-article","article-title":"Remodelling the extracellular matrix in development and disease","volume":"15","author":"Bonnans","year":"2014","journal-title":"Nature Reviews. Molecular Cell Biology"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1016\/j.molcel.2020.07.001","type":"journal-article","article-title":"Kinase interaction network expands functional and disease roles of human kinases","volume":"79","author":"Buljan","year":"2020","journal-title":"Molecular Cell"},{"key":"bib15","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a004960","type":"journal-article","article-title":"Tenascins and the importance of adhesion modulation","volume":"3","author":"Chiquet-Ehrismann","year":"2011","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1093\/brain\/awr357","type":"journal-article","article-title":"Cobblestone lissencephaly: neuropathological subtypes and correlations with genes of dystroglycanopathies","volume":"135","author":"Devisme","year":"2012","journal-title":"Brain"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1055\/s-2007-979744","type":"journal-article","article-title":"Lissencephaly and other malformations of cortical development: 1995 update","volume":"26","author":"Dobyns","year":"1995","journal-title":"Neuropediatrics"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.1074\/jbc.M106628200","type":"journal-article","article-title":"The human EMAP-like protein-70 (ELP70) is a microtubule destabilizer that localizes to the mitotic apparatus","volume":"277","author":"Eichenmuller","year":"2002","journal-title":"The Journal of Biological Chemistry"},{"key":"bib19","doi-asserted-by":"publisher","DOI":"10.1038\/msb4100134","type":"journal-article","article-title":"Large-scale mapping of human protein-protein interactions by mass spectrometry","volume":"3","author":"Ewing","year":"2007","journal-title":"Molecular Systems Biology"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1002\/dneu.20946","type":"journal-article","article-title":"Extracellular matrix functions during neuronal migration and lamination in the mammalian central nervous system","volume":"71","author":"Franco","year":"2011","journal-title":"Developmental Neurobiology"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1038\/ejhg.2010.28","type":"journal-article","article-title":"Heterozygous deletion of a 2-Mb region including the dystroglycan gene in a patient with mild myopathy, facial hypotonia, oral-motor dyspraxia and white matter abnormalities","volume":"18","author":"Frost","year":"2010","journal-title":"European Journal of Human Genetics"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1042\/BST20160125","type":"journal-article","article-title":"EML proteins in microtubule regulation and human disease","volume":"44","author":"Fry","year":"2016","journal-title":"Biochemical Society Transactions"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1007\/s10048-013-0374-9","type":"journal-article","article-title":"Homozygous dystroglycan mutation associated with a novel muscle-eye-brain disease-like phenotype with multicystic leucodystrophy","volume":"14","author":"Geis","year":"2013","journal-title":"Neurogenetics"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"2725","DOI":"10.1093\/brain\/awm212","type":"journal-article","article-title":"Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan","volume":"130","author":"Godfrey","year":"2007","journal-title":"Brain"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1016\/j.molcel.2023.01.015","type":"journal-article","article-title":"Multiplexed kinase interactome profiling quantifies cellular network activity and plasticity","volume":"83","author":"Golkowski","year":"2023","journal-title":"Molecular Cell"},{"key":"bib26","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a022608","type":"journal-article","article-title":"Microtubules and microtubule-associated proteins","volume":"10","author":"Goodson","year":"2018","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/nrm1739","type":"journal-article","article-title":"The cell biology of neurogenesis","volume":"6","author":"G\u00f6tz","year":"2005","journal-title":"Nature Reviews. Molecular Cell Biology"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1038\/nrn3586","type":"journal-article","article-title":"Molecular logic of neocortical projection neuron specification, development and diversity","volume":"14","author":"Greig","year":"2013","journal-title":"Nature Reviews. Neuroscience"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1177\/08830738050200040401","type":"journal-article","article-title":"Neuronal migration disorders, genetics, and epileptogenesis","volume":"20","author":"Guerrini","year":"2005","journal-title":"Journal of Child Neurology"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1007\/s00221-006-0501-z","type":"journal-article","article-title":"Genetic malformations of cortical development","volume":"173","author":"Guerrini","year":"2006","journal-title":"Experimental Brain Research"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1016\/S1474-4422(14)70040-7","type":"journal-article","article-title":"Malformations of cortical development: clinical features and genetic causes","volume":"13","author":"Guerrini","year":"2014","journal-title":"The Lancet. Neurology"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1038\/nrg799","type":"journal-article","article-title":"Life is a journey: a genetic look at neocortical development","volume":"3","author":"Gupta","year":"2002","journal-title":"Nature Reviews. Genetics"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"6029","DOI":"10.1523\/JNEUROSCI.22-14-06029.2002","type":"journal-article","article-title":"A critical function of the pial basement membrane in cortical histogenesis","volume":"22","author":"Halfter","year":"2002","journal-title":"The Journal of Neuroscience"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1038\/nrn3915","type":"journal-article","article-title":"Development, evolution and pathology of neocortical subplate neurons","volume":"16","author":"Hoerder-Suabedissen","year":"2015","journal-title":"Nature Reviews. Neuroscience"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"1373","DOI":"10.1016\/j.neuroscience.2006.11.015","type":"journal-article","article-title":"Echinoderm microtubule-associated protein like protein 4, a member of the echinoderm microtubule-associated protein family, stabilizes microtubules","volume":"144","author":"Houtman","year":"2007","journal-title":"Neuroscience"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1126\/science.1181348","type":"journal-article","article-title":"Systematic analysis of human protein complexes identifies chromosome segregation proteins","volume":"328","author":"Hutchins","year":"2010","journal-title":"Science"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1016\/j.cell.2021.04.011","type":"journal-article","article-title":"Dual proteome-scale networks reveal cell-specific remodeling of the human interactome","volume":"184","author":"Huttlin","year":"2021","journal-title":"Cell"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"4564","DOI":"10.3390\/ijms13044564","type":"journal-article","article-title":"Cell adhesion and its endocytic regulation in cell migration during neural development and cancer metastasis","volume":"13","author":"Kawauchi","year":"2012","journal-title":"International Journal of Molecular Sciences"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1038\/nn.3729","type":"journal-article","article-title":"Mutations in Eml1 lead to ectopic progenitors and neuronal heterotopia in mouse and human","volume":"17","author":"Kielar","year":"2014","journal-title":"Nature Neuroscience"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1038\/nrn2008","type":"journal-article","article-title":"Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion","volume":"7","author":"Kriegstein","year":"2006","journal-title":"Nature Reviews. Neuroscience"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1146\/annurev.neuro.051508.135600","type":"journal-article","article-title":"The glial nature of embryonic and adult neural stem cells","volume":"32","author":"Kriegstein","year":"2009","journal-title":"Annual Review of Neuroscience"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"47","DOI":"10.31887\/DCNS.2008.10.1\/rjleventer","type":"journal-article","article-title":"Malformations of cortical development and epilepsy","volume":"10","author":"Leventer","year":"2008","journal-title":"Dialogues in Clinical Neuroscience"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"5817","DOI":"10.1523\/JNEUROSCI.0853-08.2008","type":"journal-article","article-title":"GPR56 regulates pial basement membrane integrity and cortical lamination","volume":"28","author":"Li","year":"2008","journal-title":"The Journal of Neuroscience"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"1240","DOI":"10.1177\/1535370219867296","type":"journal-article","article-title":"Microtubules: Evolving roles and critical cellular interactions","volume":"244","author":"Logan","year":"2019","journal-title":"Experimental Biology and Medicine"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"12925","DOI":"10.1073\/pnas.1104821108","type":"journal-article","article-title":"G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination","volume":"108","author":"Luo","year":"2011","journal-title":"PNAS"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"5643","DOI":"10.1074\/jbc.RA118.007164","type":"journal-article","article-title":"The microtubule-associated protein EML3 regulates mitotic spindle assembly by recruiting the Augmin complex to spindle microtubules","volume":"294","author":"Luo","year":"2019","journal-title":"The Journal of Biological Chemistry"},{"key":"bib47","doi-asserted-by":"publisher","DOI":"10.3389\/fnins.2015.00098","type":"journal-article","article-title":"Proteoglycans and neuronal migration in the cerebral cortex during development and disease","volume":"9","author":"Maeda","year":"2015","journal-title":"Frontiers in Neuroscience"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"1802","DOI":"10.1212\/01.wnl.0000346518.68110.60","type":"journal-article","article-title":"Congenital muscular dystrophies with defective glycosylation of dystroglycan: a population study","volume":"72","author":"Mercuri","year":"2009","journal-title":"Neurology"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"3133","DOI":"10.1242\/dev.01173","type":"journal-article","article-title":"Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells","volume":"131","author":"Miyata","year":"2004","journal-title":"Development"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"1480","DOI":"10.1128\/MCB.00651-07","type":"journal-article","article-title":"Galpha12\/Galpha13 deficiency causes localized overmigration of neurons in the developing cerebral and cerebellar cortices","volume":"28","author":"Moers","year":"2008","journal-title":"Molecular and Cellular Biology"},{"key":"bib51","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1038\/nature00838","type":"journal-article","article-title":"Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy","volume":"418","author":"Moore","year":"2002","journal-title":"Nature"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1097\/NEN.0b013e318274a128","type":"journal-article","article-title":"Dystroglycan on radial glia end feet is required for pial basement membrane integrity and columnar organization of the developing cerebral cortex","volume":"71","author":"Myshrall","year":"2012","journal-title":"Journal of Neuropathology and Experimental Neurology"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1002\/cne.20322","type":"journal-article","article-title":"Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex","volume":"479","author":"Nieto","year":"2004","journal-title":"The Journal of Comparative Neurology"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/nn1172","type":"journal-article","article-title":"Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases","volume":"7","author":"Noctor","year":"2004","journal-title":"Nature Neuroscience"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1002\/cne.21669","type":"journal-article","article-title":"Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis","volume":"508","author":"Noctor","year":"2008","journal-title":"The Journal of Comparative Neurology"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"3241","DOI":"10.1016\/j.yexcr.2006.06.035","type":"journal-article","article-title":"Human EML4, a novel member of the EMAP family, is essential for microtubule formation","volume":"312","author":"Pollmann","year":"2006","journal-title":"Experimental Cell Research"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1016\/j.ajhg.2013.02.005","type":"journal-article","article-title":"Mutations in LAMB1 cause cobblestone brain malformation without muscular or ocular abnormalities","volume":"92","author":"Radmanesh","year":"2013","journal-title":"American Journal of Human Genetics"},{"key":"bib58","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0018818","type":"journal-article","article-title":"Directed evolution reveals the binding motif preference of the LC8\/DYNLL hub protein and predicts large numbers of novel binders in the human proteome","volume":"6","author":"Rapali","year":"2011","journal-title":"PLOS ONE"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"5195","DOI":"10.1073\/pnas.1322892111","type":"journal-article","article-title":"Crystal structure of EML1 reveals the basis for Hsp90 dependence of oncogenic EML4-ALK by disruption of an atypical \u03b2-propeller domain","volume":"111","author":"Richards","year":"2014","journal-title":"PNAS"},{"key":"bib60","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1042\/BJ20150039","type":"journal-article","article-title":"Microtubule association of EML proteins and the EML4-ALK variant 3 oncoprotein require an N-terminal trimerization domain","volume":"467","author":"Richards","year":"2015","journal-title":"The Biochemical Journal"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"2177","DOI":"10.1212\/WNL.0000000000001615","type":"journal-article","article-title":"Absence of \u03b1- and \u03b2-dystroglycan is associated with Walker-Warburg syndrome","volume":"84","author":"Riemersma","year":"2015","journal-title":"Neurology"},{"key":"bib62","doi-asserted-by":"publisher","first-page":"R242","DOI":"10.1016\/s0960-9822(99)80153-5","type":"journal-article","article-title":"Basement membranes: Putting up the barriers","volume":"9","author":"Schwarzbauer","year":"1999","journal-title":"Current Biology"},{"key":"bib63","doi-asserted-by":"publisher","first-page":"890","DOI":"10.1002\/ana.24964","type":"journal-article","article-title":"The genetic landscape of familial congenital hydrocephalus","volume":"81","author":"Shaheen","year":"2017","journal-title":"Annals of Neurology"},{"key":"bib64","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1016\/j.gde.2010.12.005","type":"journal-article","article-title":"We have got you \u201ccovered\u201d: how the meninges control brain development","volume":"21","author":"Siegenthaler","year":"2011","journal-title":"Current Opinion in Genetics & Development"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1007\/BF01183867","type":"journal-article","article-title":"Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane","volume":"23","author":"Sievers","year":"1994","journal-title":"Journal of Neurocytology"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1038\/nature10163","type":"journal-article","article-title":"A conditional knockout resource for the genome-wide study of mouse gene function","volume":"474","author":"Skarnes","year":"2011","journal-title":"Nature"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1634\/stemcells.2008-0319","type":"journal-article","article-title":"A Sox1 to Pax6 switch drives neuroectoderm to radial glia progression during differentiation of mouse embryonic stem cells","volume":"27","author":"Suter","year":"2009","journal-title":"Stem Cells"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1016\/j.neuron.2010.08.027","type":"journal-article","article-title":"Neural progenitor nuclei IN motion","volume":"67","author":"Taverna","year":"2010","journal-title":"Neuron"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"1718","DOI":"10.1242\/jcs.019174","type":"journal-article","article-title":"EML3 is a nuclear microtubule-binding protein required for the correct alignment of chromosomes in metaphase","volume":"121","author":"Tegha-Dunghu","year":"2008","journal-title":"Journal of Cell Science"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1038\/ng1169","type":"journal-article","article-title":"14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome","volume":"34","author":"Toyo-oka","year":"2003","journal-title":"Nature Genetics"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1152\/physrev.00040.2007","type":"journal-article","article-title":"Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases","volume":"89","author":"Turgeon","year":"2009","journal-title":"Physiological Reviews"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.conb.2009.12.003","type":"journal-article","article-title":"Neuronal migration mechanisms in development and disease","volume":"20","author":"Valiente","year":"2010","journal-title":"Current Opinion in Neurobiology"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1111\/j.1399-0004.2004.00368.x","type":"journal-article","article-title":"Glyc-O-genetics of Walker-Warburg syndrome","volume":"67","author":"van Reeuwijk","year":"2005","journal-title":"Clinical Genetics"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1136\/jmg.2005.031963","type":"journal-article","article-title":"POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome","volume":"42","author":"van Reeuwijk","year":"2005","journal-title":"Journal of Medical Genetics"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"2711","DOI":"10.1242\/dev.129.11.2711","type":"journal-article","article-title":"Specific ablation of the nidogen-binding site in the laminin gamma1 chain interferes with kidney and lung development","volume":"129","author":"Willem","year":"2002","journal-title":"Development"},{"key":"bib76","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.03941","type":"journal-article","article-title":"The glucuronyltransferase B4GAT1 is required for initiation of LARGE-mediated \u03b1-dystroglycan functional glycosylation","volume":"3","author":"Willer","year":"2014","journal-title":"eLife"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1046\/j.1440-169X.1998.00003.x","type":"journal-article","article-title":"Combinatorial expression patterns of individual TLE proteins during cell determination and differentiation suggest non\u2010redundant functions for mammalian homologs of    Drosophila    Groucho","volume":"40","author":"Yao","year":"1998","journal-title":"Development, Growth & Differentiation"},{"key":"bib78","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/bs.ctm.2015.05.001","type":"journal-article","article-title":"Integrating activities of laminins that drive basement membrane assembly and function","volume":"76","author":"Yurchenco","year":"2015","journal-title":"Current Topics in Membranes"},{"key":"bib79","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.202310157","type":"journal-article","article-title":"Forebrain Eml1 depletion reveals early centrosomal dysfunction causing subcortical heterotopia","volume":"223","author":"Zaidi","year":"2024","journal-title":"The Journal of Cell Biology"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/107102\/elife-107102-v1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/107102\/elife-107102-v1.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/107102","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T08:55:59Z","timestamp":1787561759000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/107102"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,9]]},"references-count":79,"alternative-id":["10.7554\/eLife.107102"],"URL":"https:\/\/doi.org\/10.7554\/elife.107102","archive":["CLOCKSS"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.04.06.647459","asserted-by":"subject"}],"is-same-as":[{"id-type":"doi","id":"10.7554\/eLife.107102.3","asserted-by":"subject"}],"is-version-of":[{"id-type":"doi","id":"10.7554\/eLife.107102.1","asserted-by":"subject"},{"id-type":"doi","id":"10.7554\/eLife.107102.2","asserted-by":"subject"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,9]]},"assertion":[{"value":"single anonymised","name":"peer_review_transparency","label":"Peer review transparency","group":{"name":"peer_review_taxonomy"}},{"value":"other reviewer(s), editor","name":"peer_review_interaction","label":"Peer review interaction","group":{"name":"peer_review_taxonomy"}},{"value":"review summaries, review reports, author\/editor communication, reviewer identities reviewer opt in, editor identities","name":"peer_review_published","label":"Peer review published","group":{"name":"peer_review_taxonomy"}},{"value":"open (sign in with ORCID iD required)","name":"post_publication_commenting","label":"Post publication commenting","group":{"name":"post_publication_commenting"}}],"article-number":"RP107102"}}