{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T14:29:06Z","timestamp":1782484146938,"version":"3.54.5"},"reference-count":52,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"funder":[{"DOI":"10.13039\/100012910","name":"National Defense Medical College","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100012910","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Experimental Eye Research"],"published-print":{"date-parts":[[2021,4]]},"DOI":"10.1016\/j.exer.2021.108490","type":"journal-article","created":{"date-parts":[[2021,2,16]],"date-time":"2021-02-16T08:42:42Z","timestamp":1613464962000},"page":"108490","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":29,"special_numbering":"C","title":["Microglia increase tight-junction permeability in coordination with M\u00fcller cells under hypoxic condition in an in vitro model of inner blood-retinal barrier"],"prefix":"10.1016","volume":"205","author":[{"given":"Makoto","family":"Inada","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4000-931X","authenticated-orcid":false,"given":"Heping","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4913-7089","authenticated-orcid":false,"given":"Masaru","family":"Takeuchi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masataka","family":"Ito","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5661-1386","authenticated-orcid":false,"given":"Mei","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.exer.2021.108490_bib1","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.nbd.2009.07.030","article-title":"Structure and function of the blood-brain barrier","volume":"37","author":"Abbott","year":"2010","journal-title":"Neurobiol. Dis."},{"key":"10.1016\/j.exer.2021.108490_bib2","first-page":"451","article-title":"Modulation of retinal capillary endothelial cells by Muller glial cell-derived factors","volume":"15","author":"Abukawa","year":"2009","journal-title":"Mol. Vis."},{"key":"10.1016\/j.exer.2021.108490_bib3","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/S0039-6257(03)00030-4","article-title":"Age-related macular degeneration: etiology, pathogenesis, and therapeutic strategies","volume":"48","author":"Ambati","year":"2003","journal-title":"Surv. Ophthalmol."},{"key":"10.1016\/j.exer.2021.108490_bib4","doi-asserted-by":"crossref","first-page":"2454","DOI":"10.1172\/JCI60842","article-title":"Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease","volume":"122","author":"Argaw","year":"2012","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.exer.2021.108490_bib5","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1186\/s12974-019-1625-y","article-title":"IL-33 deficiency causes persistent inflammation and severe neurodegeneration in retinal detachment","volume":"16","author":"Augustine","year":"2019","journal-title":"J. Neuroinflammation"},{"key":"10.1016\/j.exer.2021.108490_bib6","doi-asserted-by":"crossref","first-page":"1666","DOI":"10.1167\/iovs.17-23293","article-title":"Characterization of a spontaneously immortalized murine muller glial cell line QMMuC-1","volume":"59","author":"Augustine","year":"2018","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"10.1016\/j.exer.2021.108490_bib7","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1002\/path.2611","article-title":"Muller cell-derived VEGF is a significant contributor to retinal neovascularization","volume":"219","author":"Bai","year":"2009","journal-title":"J. Pathol."},{"key":"10.1016\/j.exer.2021.108490_bib8","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/j.preteyeres.2006.05.003","article-title":"Muller cells in the healthy and diseased retina","volume":"25","author":"Bringmann","year":"2006","journal-title":"Prog. Retin. Eye Res."},{"key":"10.1016\/j.exer.2021.108490_bib9","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.brainresrev.2010.05.003","article-title":"Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches","volume":"64","author":"Cardoso","year":"2010","journal-title":"Brain Res. Rev."},{"key":"10.1016\/j.exer.2021.108490_bib10","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1002\/ana.23648","article-title":"The blood-brain barrier in health and disease","volume":"72","author":"Daneman","year":"2012","journal-title":"Ann. Neurol."},{"key":"10.1016\/j.exer.2021.108490_bib11","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1007\/s00401-015-1524-y","article-title":"Microglia-blood vessel interactions: a double-edged sword in brain pathologies","volume":"131","author":"Dudvarski Stankovic","year":"2016","journal-title":"Acta Neuropathol."},{"key":"10.1016\/j.exer.2021.108490_bib12","first-page":"668","article-title":"Vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor: implications for ocular angiogenesis","volume":"137","author":"Duh","year":"2004","journal-title":"Am. J. Ophthalmol."},{"key":"10.1016\/j.exer.2021.108490_bib13","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.yexcr.2004.05.020","article-title":"PEDF derived from glial M\u00fcller cells: a possible regulator of retinal angiogenesis","volume":"299","author":"Eichler","year":"2004","journal-title":"Exp. Cell Res."},{"key":"10.1016\/j.exer.2021.108490_bib14","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1097\/01.wnr.0000133071.00786.a4","article-title":"Angiogenesis-related factors derived from retinal glial (M\u00fcller) cells in hypoxia","volume":"15","author":"Eichler","year":"2004","journal-title":"Neuroreport"},{"key":"10.1016\/j.exer.2021.108490_bib15","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1146\/annurev.med.58.061705.145635","article-title":"Targeting VEGF-A to treat cancer and age-related macular degeneration","volume":"58","author":"Ferrara","year":"2007","journal-title":"Annu. Rev. Med."},{"key":"10.1016\/j.exer.2021.108490_bib16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0079-6107(02)00037-8","article-title":"Tight junction proteins","volume":"81","author":"Gonzalez-Mariscal","year":"2003","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"10.1016\/j.exer.2021.108490_bib17","doi-asserted-by":"crossref","first-page":"4","DOI":"10.2174\/1874364101307010004","article-title":"Diabetic retinopathy and VEGF","volume":"7","author":"Gupta","year":"2013","journal-title":"Open Ophthalmol. J."},{"key":"10.1016\/j.exer.2021.108490_bib18","doi-asserted-by":"crossref","first-page":"51","DOI":"10.3325\/cmj.2016.57.51","article-title":"Hyperbaric oxygen preconditioning ameliorates blood-brain barrier damage induced by hypoxia through modulation of tight junction proteins in an in vitro model","volume":"57","author":"Hao","year":"2016","journal-title":"Croat. Med. J."},{"key":"10.1016\/j.exer.2021.108490_bib19","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1124\/pr.57.2.4","article-title":"The blood-brain barrier\/neurovascular unit in health and disease","volume":"57","author":"Hawkins","year":"2005","journal-title":"Pharmacol. Rev."},{"key":"10.1016\/j.exer.2021.108490_bib20","doi-asserted-by":"crossref","first-page":"9103","DOI":"10.1073\/pnas.1821122116","article-title":"Hypoxia tolerance in the Norrin-deficient retina and the chronically hypoxic brain studied at single-cell resolution","volume":"116","author":"Heng","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.exer.2021.108490_bib21","doi-asserted-by":"crossref","first-page":"6974","DOI":"10.3892\/mmr.2017.7475","article-title":"FK506 suppresses hypoxiainduced inflammation and protects tight junction function via the CaNNFATc1 signaling pathway in retinal microvascular epithelial cells","volume":"16","author":"Hu","year":"2017","journal-title":"Mol. Med. Rep."},{"key":"10.1016\/j.exer.2021.108490_bib22","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1247\/csf.25.237","article-title":"Expression of receptors for glial cell line-derived neurotrophic factor (GDNF) and neurturin in the inner blood-retinal barrier of rats","volume":"25","author":"Igarashi","year":"2000","journal-title":"Cell Struct. Funct."},{"key":"10.1016\/j.exer.2021.108490_bib23","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.exer.2018.09.014","article-title":"Protective effects of dexamethasone on hypoxia-induced retinal edema in a mouse model","volume":"178","author":"Inada","year":"2018","journal-title":"Exp. Eye Res."},{"key":"10.1016\/j.exer.2021.108490_bib24","doi-asserted-by":"crossref","first-page":"2115","DOI":"10.1096\/fj.03-0329fje","article-title":"IL-1beta-mediated up-regulation of HIF-1alpha via an NFkappaB\/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis","volume":"17","author":"Jung","year":"2003","journal-title":"Faseb. J. : Off. Publ. Feder. Am. Soc. Exper. Biol."},{"key":"10.1016\/j.exer.2021.108490_bib25","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/1476-9255-8-7","article-title":"Endotoxin-activated microglia injure brain derived endothelial cells via NF-kappaB, JAK-STAT and JNK stress kinase pathways","volume":"8","author":"Kacimi","year":"2011","journal-title":"J. Inflamm. (Lond., England)"},{"key":"10.1016\/j.exer.2021.108490_bib26","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s11481-012-9347-2","article-title":"Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina","volume":"8","author":"Kaur","year":"2013","journal-title":"J. Neuroimmune Pharmacol. : Off. J. Soc. NeuroImm. Pharmacol."},{"key":"10.1016\/j.exer.2021.108490_bib27","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1167\/iovs.05-0518","article-title":"Early response of neurons and glial cells to hypoxia in the retina","volume":"47","author":"Kaur","year":"2006","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"10.1016\/j.exer.2021.108490_bib28","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1152\/physrev.00011.2010","article-title":"Physiology of microglia","volume":"91","author":"Kettenmann","year":"2011","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.exer.2021.108490_bib29","doi-asserted-by":"crossref","first-page":"1389","DOI":"10.2353\/ajpath.2007.060693","article-title":"Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells","volume":"170","author":"Koto","year":"2007","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.exer.2021.108490_bib30","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.18240\/ijo.2020.09.04","article-title":"Acetylcholinesterase inhibition ameliorates retinal neovascularization and glial activation in oxygen-induced retinopathy","volume":"13","author":"Liu","year":"2020","journal-title":"Int. J. Ophthalmol."},{"key":"10.1016\/j.exer.2021.108490_bib31","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0082604","article-title":"Hypoxia\/Aglycemia-induced endothelial barrier dysfunction and tight junction protein downregulation can be ameliorated by citicoline","volume":"8","author":"Ma","year":"2013","journal-title":"PloS One"},{"key":"10.1016\/j.exer.2021.108490_bib32","doi-asserted-by":"crossref","first-page":"H1485","DOI":"10.1152\/ajpheart.00645.2001","article-title":"Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation","volume":"282","author":"Mark","year":"2002","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"10.1016\/j.exer.2021.108490_bib33","first-page":"1411","article-title":"Pathophysiologic effect of interleukin-1b in the rabbit retina","volume":"137","author":"Martiney","year":"1990","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.exer.2021.108490_bib34","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1056\/NEJMoa1007374","article-title":"Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity","volume":"364","author":"Mintz-Hittner","year":"2011","journal-title":"N. Engl. J. Med."},{"key":"10.1016\/j.exer.2021.108490_bib35","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.exer.2017.10.011","article-title":"Myeloid cells contribute indirectly to VEGF expression upon hypoxia via activation of Muller cells","volume":"166","author":"Nurnberg","year":"2018","journal-title":"Exp. Eye Res."},{"key":"10.1016\/j.exer.2021.108490_bib36","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1073\/pnas.92.3.905","article-title":"Vascular endothelial growth factor\/vascular permeability factor expression in a mouse model of retinal neovascularization","volume":"92","author":"Pierce","year":"1995","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.exer.2021.108490_bib37","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1007\/s11481-014-9531-7","article-title":"Vascular endothelial growth factor signaling in hypoxia and inflammation","volume":"9","author":"Ramakrishnan","year":"2014","journal-title":"J. Neuroimmune Pharmacol. : Off. J. Soc. NeuroImm. Pharmacol."},{"key":"10.1016\/j.exer.2021.108490_bib38","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1172\/JCI58644","article-title":"Innate immunity in the central nervous system","volume":"122","author":"Ransohoff","year":"2012","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.exer.2021.108490_bib39","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1002\/glia.22477","article-title":"New functions of Muller cells","volume":"61","author":"Reichenbach","year":"2013","journal-title":"Glia"},{"key":"10.1016\/j.exer.2021.108490_bib40","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0003554","article-title":"Endogenous VEGF is required for visual function: evidence for a survival role on muller cells and photoreceptors","volume":"3","author":"Saint-Geniez","year":"2008","journal-title":"PloS One"},{"key":"10.1016\/j.exer.2021.108490_bib41","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.schres.2013.09.011","article-title":"Pretreatment of aripiprazole and minocycline, but not haloperidol, suppresses oligodendrocyte damage from interferon-gamma-stimulated microglia in co-culture model","volume":"151","author":"Seki","year":"2013","journal-title":"Schizophr. Res."},{"key":"10.1016\/j.exer.2021.108490_bib42","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1002\/path.2858","article-title":"Retinal ganglion cell death is induced by microglia derived pro-inflammatory cytokines in the hypoxic neonatal retina","volume":"224","author":"Sivakumar","year":"2011","journal-title":"J. Pathol."},{"key":"10.1016\/j.exer.2021.108490_bib43","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1172\/JCI0214362","article-title":"Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms","volume":"109","author":"Stalmans","year":"2002","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.exer.2021.108490_bib44","doi-asserted-by":"crossref","first-page":"2192","DOI":"10.1172\/JCI119392","article-title":"Vascular dysfunction induced by elevated glucose levels in rats is mediated by vascular endothelial growth factor","volume":"99","author":"Tilton","year":"1997","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.exer.2021.108490_bib45","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/0306-4522(93)90473-S","article-title":"The role of M\u00fcller cells in the formation of the blood-retinal barrier","volume":"55","author":"Tout","year":"1993","journal-title":"Neuroscience"},{"key":"10.1016\/j.exer.2021.108490_bib46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.preteyeres.2015.06.003","article-title":"Glia-neuron interactions in the mammalian retina","volume":"51","author":"Vecino","year":"2016","journal-title":"Prog. Retin. Eye Res."},{"key":"10.1016\/j.exer.2021.108490_bib47","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.exer.2013.09.014","article-title":"Hypoxia-induced expression of VEGF splice variants and protein in four retinal cell types","volume":"116","author":"Watkins","year":"2013","journal-title":"Exp. Eye Res."},{"key":"10.1016\/j.exer.2021.108490_bib48","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1002\/glia.22988","article-title":"Targeting microglia for the treatment of Alzheimer's Disease","volume":"64","author":"Wes","year":"2016","journal-title":"Glia"},{"key":"10.1016\/j.exer.2021.108490_bib49","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/S1537-1891(02)00200-8","article-title":"Tight junctions of the blood-brain barrier: development, composition and regulation","volume":"38","author":"Wolburg","year":"2002","journal-title":"Vasc. Pharmacol."},{"key":"10.1016\/j.exer.2021.108490_bib50","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/BF00691332","article-title":"Evaluation of the dye-protein tracers in pathophysiology of the blood-brain barrier","volume":"54","author":"Wolman","year":"1981","journal-title":"Acta Neuropathol."},{"key":"10.1016\/j.exer.2021.108490_bib51","doi-asserted-by":"crossref","first-page":"99","DOI":"10.2147\/EB.S9078","article-title":"Energy metabolism of the visual system","volume":"2","author":"Wong-Riley","year":"2010","journal-title":"Eye Brain"},{"key":"10.1016\/j.exer.2021.108490_bib52","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1007\/s00011-010-0207-3","article-title":"Role of src-suppressed C kinase substrate in rat pulmonary microvascular endothelial hyperpermeability stimulated by inflammatory cytokines","volume":"59","author":"You","year":"2010","journal-title":"Inflamm. Res. : Off. J. Eur. Histamine Res. Soc."}],"container-title":["Experimental Eye Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0014483521000555?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0014483521000555?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,16]],"date-time":"2025-09-16T05:14:13Z","timestamp":1757999653000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0014483521000555"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4]]},"references-count":52,"alternative-id":["S0014483521000555"],"URL":"https:\/\/doi.org\/10.1016\/j.exer.2021.108490","relation":{},"ISSN":["0014-4835"],"issn-type":[{"value":"0014-4835","type":"print"}],"subject":[],"published":{"date-parts":[[2021,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Microglia increase tight-junction permeability in coordination with M\u00fcller cells under hypoxic condition in an in vitro model of inner blood-retinal barrier","name":"articletitle","label":"Article Title"},{"value":"Experimental Eye Research","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.exer.2021.108490","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 Elsevier Ltd. All rights reserved.","name":"copyright","label":"Copyright"}],"article-number":"108490"}}