{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T19:02:52Z","timestamp":1790276572701,"version":"4.1.0"},"reference-count":55,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100008136","name":"Case Western Reserve University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008136","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neurobiology of Disease"],"published-print":{"date-parts":[[2021,7]]},"DOI":"10.1016\/j.nbd.2021.105339","type":"journal-article","created":{"date-parts":[[2021,3,26]],"date-time":"2021-03-26T19:11:44Z","timestamp":1616785904000},"page":"105339","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":26,"special_numbering":"C","title":["Linking cortical astrocytic neogenin deficiency to the development of Moyamoya disease\u2013like vasculopathy"],"prefix":"10.1016","volume":"154","author":[{"given":"Xiao","family":"Ren","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling-Ling","family":"Yao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin-Xiu","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun-Shi","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Mei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong-Gang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Cheng","family":"Xiong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.nbd.2021.105339_bb0005","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1007\/s12079-016-0352-8","article-title":"VEGF-A\/VEGFR2 signaling network in endothelial cells relevant to angiogenesis","volume":"10","author":"Abhinand","year":"2016","journal-title":"Journal of cell communication and signaling."},{"key":"10.1016\/j.nbd.2021.105339_bb0010","doi-asserted-by":"crossref","first-page":"E1289","DOI":"10.1073\/pnas.1710329115","article-title":"Tau induces blood vessel abnormalities and angiogenesis-related gene expression in P301L transgenic mice and human Alzheimer\u2019s disease","volume":"115","author":"Bennett","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.nbd.2021.105339_bb0015","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.atherosclerosis.2020.02.015","article-title":"The identification and function of a Netrin-1 mutation in a pedigree with premature atherosclerosis","volume":"301","author":"Bruikman","year":"2020","journal-title":"Atherosclerosis."},{"key":"10.1016\/j.nbd.2021.105339_bb0020","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.1161\/01.STR.29.7.1347","article-title":"Clinical features of moyamoya disease in the United States","volume":"29","author":"Chiu","year":"1998","journal-title":"Stroke."},{"key":"10.1016\/j.nbd.2021.105339_bb0025","doi-asserted-by":"crossref","first-page":"135","DOI":"10.3109\/03009734.2015.1064501","article-title":"Vascular permeability\u2014the essentials","volume":"120","author":"Claesson-Welsh","year":"2015","journal-title":"Ups. J. Med. Sci."},{"key":"10.1016\/j.nbd.2021.105339_bb0030","series-title":"Neogenin: A Multi-Functional Receptor Regulating Diverse Developmental Processes","first-page":"1569","volume":"39","author":"Cole","year":"2007"},{"key":"10.1016\/j.nbd.2021.105339_bb0035","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1038\/nn1144","article-title":"The glial identity of neural stem cells","volume":"6","author":"Doetsch","year":"2003","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.nbd.2021.105339_bb0040","series-title":"Signal Processing Methods for Quantitative Power Doppler Microvascular Angiography","first-page":"3106","author":"Elfarnawany","year":"2015"},{"key":"10.1016\/j.nbd.2021.105339_bb0045","doi-asserted-by":"crossref","first-page":"35104","DOI":"10.1074\/jbc.M112.363937","article-title":"Neogenin interacts with Matriptase-2 to facilitate Hemojuvelin cleavage","volume":"287","author":"Enns","year":"2012","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.nbd.2021.105339_bb0050","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1007\/s00415-009-5424-8","article-title":"Neurocognitive dysfunction in adult moyamoya disease","volume":"257","author":"Festa","year":"2010","journal-title":"J. Neurol."},{"key":"10.1016\/j.nbd.2021.105339_bb0055","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1161\/01.ATV.0000070546.16946.3A","article-title":"Caveolin, caveolae, and endothelial cell function","volume":"23","author":"Frank","year":"2003","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"10.1016\/j.nbd.2021.105339_bb0060","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s41232-017-0037-6","article-title":"The roles of RGMa-neogenin signaling in inflammation and angiogenesis","volume":"37","author":"Fujita","year":"2017","journal-title":"Inflammation and regeneration."},{"key":"10.1016\/j.nbd.2021.105339_bb0065","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1038\/jcbfm.2012.152","article-title":"In vivo imaging of cerebral microvascular plasticity from birth to death","volume":"33","author":"Harb","year":"2013","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"10.1016\/j.nbd.2021.105339_bb0070","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1007\/s12975-010-0049-x","article-title":"High and low molecular weight fluorescein isothiocyanate (FITC)\u2013dextrans to assess blood-brain barrier disruption: technical considerations","volume":"2","author":"Hoffmann","year":"2011","journal-title":"Transl. Stroke Res."},{"key":"10.1016\/j.nbd.2021.105339_bb0075","article-title":"Neogenin-YAP signaling in neocortical astrocytic differentiation","volume":"3","author":"Huang","year":"2016","journal-title":"Neurogenesis (Austin)."},{"key":"10.1016\/j.nbd.2021.105339_bb0080","doi-asserted-by":"crossref","first-page":"5833","DOI":"10.1523\/JNEUROSCI.4487-15.2016","article-title":"Neogenin promotes BMP2 activation of YAP and Smad1 and enhances astrocytic differentiation in developing mouse neocortex","volume":"36","author":"Huang","year":"2016","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2021.105339_bb0085","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.brainres.2014.11.014","article-title":"Enhanced post-ischemic angiogenesis in mice lacking RNF213; a susceptibility gene for moyamoya disease","volume":"1594","author":"Ito","year":"2015","journal-title":"Brain Res."},{"key":"10.1016\/j.nbd.2021.105339_bb0090","doi-asserted-by":"crossref","first-page":"e694","DOI":"10.1542\/peds.2005-0568","article-title":"Moyamoya syndrome associated with Down syndrome: outcome after surgical revascularization","volume":"116","author":"Jea","year":"2005","journal-title":"Pediatrics"},{"key":"10.1016\/j.nbd.2021.105339_bb0095","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1227\/NEU.0b013e31827b9beb","article-title":"Prevalence and characteristics of concurrent down syndrome in patients with moyamoya disease","volume":"72","author":"Kainth","year":"2013","journal-title":"Neurosurgery."},{"issue":"Suppl3","key":"10.1016\/j.nbd.2021.105339_bb0100","doi-asserted-by":"crossref","first-page":"S115","DOI":"10.1097\/00002093-199912003-00017","article-title":"Overlap between pathology of Alzheimer disease and vascular dementia","volume":"13","author":"Kalaria","year":"1999","journal-title":"Alzheimer Dis. Assoc. Disord."},{"key":"10.1016\/j.nbd.2021.105339_bb0105","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1038\/jhg.2010.132","article-title":"A genome-wide association study identifies RNF213 as the first Moyamoya disease gene","volume":"56","author":"Kamada","year":"2011","journal-title":"J. Hum. Genet."},{"key":"10.1016\/j.nbd.2021.105339_bb0110","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1136\/jnnp.2009.191817","article-title":"Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease","volume":"81","author":"Kang","year":"2010","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"10.1016\/j.nbd.2021.105339_bb0115","doi-asserted-by":"crossref","first-page":"415","DOI":"10.3171\/2013.9.JNS131000","article-title":"Smooth-muscle progenitor cells isolated from patients with moyamoya disease: novel experimental cell model","volume":"120","author":"Kang","year":"2014","journal-title":"J. Neurosurg."},{"key":"10.1016\/j.nbd.2021.105339_bb0120","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1161\/STROKEAHA.114.007407","article-title":"Chronic ischemia alters brain microstructural integrity and cognitive performance in adult moyamoya disease","volume":"46","author":"Kazumata","year":"2015","journal-title":"Stroke."},{"key":"10.1016\/j.nbd.2021.105339_bb0125","doi-asserted-by":"crossref","first-page":"2","DOI":"10.5853\/jos.2015.01627","article-title":"Moyamoya disease: epidemiology, clinical features, and diagnosis","volume":"18","author":"Kim","year":"2016","journal-title":"Journal of stroke."},{"key":"10.1016\/j.nbd.2021.105339_bb0130","first-page":"e1088","article-title":"Elevated plus maze for mice","volume":"22","author":"Komada","year":"2008","journal-title":"J Vis Exp."},{"key":"10.1016\/j.nbd.2021.105339_bb0135","doi-asserted-by":"crossref","first-page":"2433","DOI":"10.1101\/gad.437807","article-title":"Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis","volume":"21","author":"Larrivee","year":"2007","journal-title":"Genes Dev."},{"key":"10.1016\/j.nbd.2021.105339_bb0140","doi-asserted-by":"crossref","first-page":"12491","DOI":"10.1073\/pnas.0804008105","article-title":"Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B","volume":"105","author":"Lejmi","year":"2008","journal-title":"Proc. Natl. Acad. Sci."},{"key":"10.1016\/j.nbd.2021.105339_bb0145","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1093\/jmcb\/mjz076","article-title":"Neogenin-loss in neural crest cells results in persistent hyperplastic primary vitreous formation","volume":"12","author":"Lin","year":"2020","journal-title":"J. Mol. Cell Biol."},{"key":"10.1016\/j.nbd.2021.105339_bb0150","series-title":"Decreased cortical perfusion in areas with blood-brain barrier dysfunction in Moyamoya disease","first-page":"1","author":"Lu","year":"2020"},{"key":"10.1016\/j.nbd.2021.105339_bb0155","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1007\/s00701-019-03811-w","article-title":"In vivo demonstration of blood-brain barrier impairment in Moyamoya disease","volume":"161","author":"Narducci","year":"2019","journal-title":"Acta Neurochir."},{"key":"10.1016\/j.nbd.2021.105339_bb0160","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/BF01664854","article-title":"Cerebral blood flow in moyamoya disease","volume":"105","author":"Ogawa","year":"1990","journal-title":"Acta Neurochir."},{"key":"10.1016\/j.nbd.2021.105339_bb0165","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/S1474-4422(10)70104-6","article-title":"Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges","volume":"9","author":"Pantoni","year":"2010","journal-title":"The Lancet Neurology."},{"key":"10.1016\/j.nbd.2021.105339_bb0170","doi-asserted-by":"crossref","first-page":"16210","DOI":"10.1073\/pnas.0405984101","article-title":"The axonal attractant Netrin-1 is an angiogenic factor","volume":"101","author":"Park","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.nbd.2021.105339_bb0175","article-title":"An in vivo assay to test blood vessel permeability","volume":"73","author":"Radu","year":"2013","journal-title":"JoVE"},{"key":"10.1016\/j.nbd.2021.105339_bb0180","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.pediatrneurol.2014.10.007","article-title":"Patterns of cerebral ischemia in children with moyamoya","volume":"52","author":"Rafay","year":"2015","journal-title":"Pediatr. Neurol."},{"key":"10.1016\/j.nbd.2021.105339_bb0185","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1038\/ncb1156","article-title":"Neogenin mediates the action of repulsive guidance molecule","volume":"6","author":"Rajagopalan","year":"2004","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.nbd.2021.105339_bb0190","doi-asserted-by":"crossref","first-page":"385","DOI":"10.3389\/fnins.2015.00385","article-title":"Markers for blood-brain barrier integrity: how appropriate is Evans blue in the twenty-first century and what are the alternatives?","volume":"9","author":"Saunders","year":"2015","journal-title":"Front. Neurosci."},{"key":"10.1016\/j.nbd.2021.105339_bb0195","first-page":"50079","article-title":"Isolation and culture of mouse cortical astrocytes","volume":"71","author":"Schildge","year":"2013","journal-title":"J Vis Exp."},{"key":"10.1016\/j.nbd.2021.105339_bb0200","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1001\/archneur.1977.00500200071015","article-title":"Moyamoya disease presenting as a seizure disorder: a case report","volume":"34","author":"Schoenberg","year":"1977","journal-title":"Arch. Neurol."},{"key":"10.1016\/j.nbd.2021.105339_bb0205","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1056\/NEJMra0804622","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"Scott","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"10.1016\/j.nbd.2021.105339_bb0210","doi-asserted-by":"crossref","first-page":"439","DOI":"10.3171\/ped.2005.103.5.0439","article-title":"Headache in pediatric moyamoya disease: review of 204 consecutive cases","volume":"103","author":"Seol","year":"2005","journal-title":"J. Neurosurg. Pediatr."},{"key":"10.1016\/j.nbd.2021.105339_bb0215","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1055\/s-2005-868160","article-title":"Surgical management of moyamoya syndrome","volume":"15","author":"Smith","year":"2005","journal-title":"Skull Base."},{"key":"10.1016\/j.nbd.2021.105339_bb0220","first-page":"719","article-title":"Delta-like ligand 4\u2013Notch signaling regulates bone marrow\u2013derived pericyte\/vascular smooth muscle cell formation","volume":"117","author":"Stewart","year":"2011","journal-title":"Blood, The Journal of the American Society of Hematology."},{"key":"10.1016\/j.nbd.2021.105339_bb0225","doi-asserted-by":"crossref","first-page":"3889","DOI":"10.4049\/jimmunol.145.11.3889","article-title":"Molecular characterization and functional analysis of the leukocyte surface protein CD31","volume":"145","author":"Stockinger","year":"1990","journal-title":"J. Immunol."},{"key":"10.1016\/j.nbd.2021.105339_bb0230","first-page":"1","article-title":"Neogenin, a regulator of adult hippocampal neurogenesis, prevents depressive-like behavior","volume":"9","author":"Sun","year":"2018","journal-title":"Cell Death Dis."},{"key":"10.1016\/j.nbd.2021.105339_bb0235","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.biopsych.2020.08.026","article-title":"Critical roles of embryonic born dorsal dentate granule neurons for activity-dependent increases in BDNF, adult hippocampal neurogenesis, and antianxiety-like behaviors","volume":"89.6","author":"Sun","year":"2021","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.nbd.2021.105339_bb0240","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1186\/s13041-015-0156-4","article-title":"VPS35-deficiency results in an impaired AMPA receptor trafficking and decreased dendritic spine maturation","volume":"8","author":"Tian","year":"2015","journal-title":"Mol Brain."},{"key":"10.1016\/j.nbd.2021.105339_bb0245","first-page":"391","article-title":"Cerebral hemodynamics in Moyamoya disease: correlation between perfusion-weighted MR imaging and cerebral angiography","volume":"27","author":"Togao","year":"2006","journal-title":"Am. J. Neuroradiol."},{"key":"10.1016\/j.nbd.2021.105339_bb0250","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1023\/A:1016581801188","article-title":"Immunogold study of interendothelial junction-associated and glucose transporter proteins during postnatal maturation of the mouse blood-brain barrier","volume":"30","author":"Vorbrodt","year":"2001","journal-title":"J. Neurocytol."},{"key":"10.1016\/j.nbd.2021.105339_bb0255","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1016\/j.ydbio.2006.06.018","article-title":"Neogenin interacts with RGMa and netrin-1 to guide axons within the embryonic vertebrate forebrain","volume":"296","author":"Wilson","year":"2006","journal-title":"Dev. Biol."},{"key":"10.1016\/j.nbd.2021.105339_bb0260","doi-asserted-by":"crossref","first-page":"6490","DOI":"10.1172\/JCI132372","article-title":"Astrocytic neogenin\/netrin-1 pathway promotes blood vessel homeostasis and function in mouse cortex","volume":"130","author":"Yao","year":"2020","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.nbd.2021.105339_bb0265","doi-asserted-by":"crossref","first-page":"1741","DOI":"10.2147\/OPTH.S258044","article-title":"Targeting netrin-1 and-4 as a novel diagnostic parameter and treatment option for diabetic retinopathy","volume":"14","author":"Zewdie","year":"2020","journal-title":"Clinical Ophthalmology (Auckland, NZ)"},{"key":"10.1016\/j.nbd.2021.105339_bb0270","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.devcel.2010.06.016","article-title":"Neogenin regulation of BMP-induced canonical Smad signaling and endochondral bone formation","volume":"19","author":"Zhou","year":"2010","journal-title":"Dev. Cell"},{"key":"10.1016\/j.nbd.2021.105339_bb0275","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1002\/gene.10008","article-title":"hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo","volume":"31","author":"Zhuo","year":"2001","journal-title":"Genesis."}],"container-title":["Neurobiology of Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996121000887?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996121000887?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,19]],"date-time":"2025-10-19T05:26:39Z","timestamp":1760851599000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0969996121000887"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7]]},"references-count":55,"alternative-id":["S0969996121000887"],"URL":"https:\/\/doi.org\/10.1016\/j.nbd.2021.105339","relation":{},"ISSN":["0969-9961"],"issn-type":[{"value":"0969-9961","type":"print"}],"subject":[],"published":{"date-parts":[[2021,7]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Linking cortical astrocytic neogenin deficiency to the development of Moyamoya disease\u2013like vasculopathy","name":"articletitle","label":"Article Title"},{"value":"Neurobiology of Disease","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.nbd.2021.105339","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"105339"}}