{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T22:17:16Z","timestamp":1792016236645,"version":"4.4.0"},"reference-count":34,"publisher":"Elsevier BV","issue":"3","license":[{"start":{"date-parts":[[2016,12,1]],"date-time":"2016-12-01T00:00:00Z","timestamp":1480550400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2016,12,1]],"date-time":"2016-12-01T00:00:00Z","timestamp":1480550400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"content-domain":{"domain":["jpet.aspetjournals.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["The Journal of Pharmacology and Experimental Therapeutics"],"published-print":{"date-parts":[[2016,12]]},"DOI":"10.1124\/jpet.116.237057","type":"journal-article","created":{"date-parts":[[2016,10,11]],"date-time":"2016-10-11T20:58:30Z","timestamp":1476219510000},"page":"452-459","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":94,"title":["Blood\u2013Brain Barrier Disruption and Neurovascular Unit Dysfunction in Diabetic Mice: Protection with the Mitochondrial Carbonic Anhydrase Inhibitor Topiramate"],"prefix":"10.1016","volume":"359","author":[{"given":"Therese S.","family":"Salameh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gul N.","family":"Shah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tulin O.","family":"Price","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melvin R.","family":"Hayden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William A.","family":"Banks","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1124\/jpet.116.237057_bib1","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1023\/A:1021067822435","article-title":"Transient forebrain ischemia increases the blood-brain barrier permeability for albumin in stroke-prone spontaneously hypertensive rats","volume":"22","author":"Abrah\u00e1m","year":"2002","journal-title":"Cell Mol Neurobiol"},{"key":"10.1124\/jpet.116.237057_bib2","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1016\/S0196-9781(97)00238-6","article-title":"Effect of diabetes mellitus on the permeability of the blood-brain barrier to insulin","volume":"18","author":"Banks","year":"1997","journal-title":"Peptides"},{"key":"10.1124\/jpet.116.237057_bib3","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.yexcr.2004.08.034","article-title":"Membrane ruffles in cell migration: indicators of inefficient lamellipodia adhesion and compartments of actin filament reorganization","volume":"302","author":"Borm","year":"2005","journal-title":"Exp Cell Res"},{"key":"10.1124\/jpet.116.237057_bib4","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1007\/s00125-002-0853-2","article-title":"Morpho-functional studies of the blood-brain barrier in streptozotocin-induced diabetic rats","volume":"45","author":"Bouchard","year":"2002","journal-title":"Diabetologia"},{"key":"10.1124\/jpet.116.237057_bib5","doi-asserted-by":"crossref","first-page":"1615","DOI":"10.2337\/diabetes.54.6.1615","article-title":"The pathobiology of diabetic complications: a unifying mechanism","volume":"54","author":"Brownlee","year":"2005","journal-title":"Diabetes"},{"key":"10.1124\/jpet.116.237057_bib6","doi-asserted-by":"crossref","first-page":"4401","DOI":"10.1210\/en.2012-1272","article-title":"Topiramate treatment improves hypothalamic insulin and leptin signaling and action and reduces obesity in mice","volume":"153","author":"Caricilli","year":"2012","journal-title":"Endocrinology"},{"key":"10.1124\/jpet.116.237057_bib7","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.jalz.2013.06.009","article-title":"Microvascular network alterations in the retina of patients with Alzheimer\u2019s disease","volume":"10","author":"Cheung","year":"2014","journal-title":"Alzheimers Dement"},{"key":"10.1124\/jpet.116.237057_bib8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00401-011-0847-6","article-title":"Brain microvascular pericytes in health and disease","volume":"122","author":"Dalkara","year":"2011","journal-title":"Acta Neuropathol"},{"key":"10.1124\/jpet.116.237057_bib9","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1038\/nature09513","article-title":"Pericytes are required for blood-brain barrier integrity during embryogenesis","volume":"468","author":"Daneman","year":"2010","journal-title":"Nature"},{"key":"10.1124\/jpet.116.237057_bib10","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.2174\/138161208784705469","article-title":"Pericytes: pluripotent cells of the blood brain barrier","volume":"14","author":"Dore-Duffy","year":"2008","journal-title":"Curr Pharm Des"},{"key":"10.1124\/jpet.116.237057_bib11","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1159\/000360101","article-title":"Coenzyme q10 therapy","volume":"5","author":"Garrido-Maraver","year":"2014","journal-title":"Mol Syndromol"},{"key":"10.1124\/jpet.116.237057_bib12","doi-asserted-by":"crossref","first-page":"912","DOI":"10.2337\/dc13-1518","article-title":"Prevention of type 2 diabetes in subjects with prediabetes and metabolic syndrome treated with phentermine and topiramate extended release","volume":"37","author":"Garvey","year":"2014","journal-title":"Diabetes Care"},{"key":"10.1124\/jpet.116.237057_bib13","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/S0166-2236(00)01656-8","article-title":"Cognition and synaptic plasticity in diabetes mellitus","volume":"23","author":"Gispen","year":"2000","journal-title":"Trends Neurosci"},{"key":"10.1124\/jpet.116.237057_bib14","doi-asserted-by":"crossref","first-page":"3107","DOI":"10.2337\/diabetes.51.10.3107","article-title":"Pericytes and the pathogenesis of diabetic retinopathy","volume":"51","author":"Hammes","year":"2002","journal-title":"Diabetes"},{"key":"10.1124\/jpet.116.237057_bib15","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1159\/000357113","article-title":"Cardiorenal metabolic syndrome and diabetic cognopathy","volume":"3","author":"Hayden","year":"2013","journal-title":"Cardiorenal Med"},{"key":"10.1124\/jpet.116.237057_bib16","doi-asserted-by":"crossref","first-page":"290","DOI":"10.4161\/oxim.3.5.13653","article-title":"Pericytopathy: oxidative stress and impaired cellular longevity in the pancreas and skeletal muscle in metabolic syndrome and type 2 diabetes","volume":"3","author":"Hayden","year":"2010","journal-title":"Oxid Med Cell Longev"},{"key":"10.1124\/jpet.116.237057_bib17","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1016\/j.jdiacomp.2013.04.011","article-title":"New options for the treatment of obesity and type 2 diabetes mellitus (narrative review)","volume":"27","author":"Henry","year":"2013","journal-title":"J Diabetes Complications"},{"key":"10.1124\/jpet.116.237057_bib18","doi-asserted-by":"crossref","first-page":"H2660","DOI":"10.1152\/ajpheart.00489.2006","article-title":"Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats","volume":"291","author":"Huber","year":"2006","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"10.1124\/jpet.116.237057_bib19","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1089\/ars.2005.7.1581","article-title":"Diabetic retinopathy: mitochondrial dysfunction and retinal capillary cell death","volume":"7","author":"Kowluru","year":"2005","journal-title":"Antioxid Redox Signal"},{"key":"10.1124\/jpet.116.237057_bib20","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1111\/j.1463-1326.2004.00403.x","article-title":"Topiramate ameliorates hyperglycaemia and improves glucose-stimulated insulin release in ZDF rats and db\/db mice","volume":"7","author":"Liang","year":"2005","journal-title":"Diabetes Obes Metab"},{"key":"10.1124\/jpet.116.237057_bib21","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.2337\/diabetes.55.04.06.db05-1323","article-title":"Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes","volume":"55","author":"Manschot","year":"2006","journal-title":"Diabetes"},{"key":"10.1124\/jpet.116.237057_bib22","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1111\/j.1600-0404.1991.tb04940.x","article-title":"Blood-brain-barrier in a geriatric population: barrier function in degenerative and vascular dementias","volume":"84","author":"Mecocci","year":"1991","journal-title":"Acta Neurol Scand"},{"key":"10.1124\/jpet.116.237057_bib23","first-page":"297","article-title":"The effect of topiramate on weight loss in patients with type 2 diabetes","volume":"18","author":"Moradi","year":"2013","journal-title":"J Res Med Sci"},{"key":"10.1124\/jpet.116.237057_bib24","doi-asserted-by":"crossref","first-page":"1937","DOI":"10.1212\/WNL.53.9.1937","article-title":"Diabetes mellitus and the risk of dementia: The Rotterdam Study","volume":"53","author":"Ott","year":"1999","journal-title":"Neurology"},{"key":"10.1124\/jpet.116.237057_bib25","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1210\/en.2011-1638","article-title":"Topiramate treatment protects blood-brain barrier pericytes from hyperglycemia-induced oxidative damage in diabetic mice","volume":"153","author":"Price","year":"2012","journal-title":"Endocrinology"},{"key":"10.1124\/jpet.116.237057_bib26","series-title":"Blood-Brain Barrier in Physiology and Medicine","first-page":"129","article-title":"Pathological alterations of the blood-brain barrier","author":"Rapoport","year":"1976"},{"key":"10.1124\/jpet.116.237057_bib27","series-title":"Advances in Pharmacology","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/bs.apha.2014.06.004","article-title":"Delivery of therapeutic peptides and proteins to the CNS","author":"Salameh","year":"2014"},{"key":"10.1124\/jpet.116.237057_bib28","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1111\/bpa.12004","article-title":"Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer\u2019s disease","volume":"23","author":"Sengillo","year":"2013","journal-title":"Brain Pathol"},{"key":"10.1124\/jpet.116.237057_bib29","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.bbrc.2013.09.086","article-title":"High glucose-induced mitochondrial respiration and reactive oxygen species in mouse cerebral pericytes is reversed by pharmacological inhibition of mitochondrial carbonic anhydrases: implications for cerebral microvascular disease in diabetes","volume":"440","author":"Shah","year":"2013","journal-title":"Biochem Biophys Res Commun"},{"key":"10.1124\/jpet.116.237057_bib30","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1124\/jpet.112.201400","article-title":"Pharmacological inhibition of mitochondrial carbonic anhydrases protects mouse cerebral pericytes from high glucose-induced oxidative stress and apoptosis","volume":"344","author":"Shah","year":"2013","journal-title":"J Pharmacol Exp Ther"},{"key":"10.1124\/jpet.116.237057_bib31","first-page":"597","article-title":"Coenzyme Q10 effects in neurodegenerative disease","volume":"5","author":"Spindler","year":"2009","journal-title":"Neuropsychiatr Dis Treat"},{"key":"10.1124\/jpet.116.237057_bib32","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1136\/jnnp.74.1.70","article-title":"Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging","volume":"74","author":"Starr","year":"2003","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"10.1124\/jpet.116.237057_bib33","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1111\/j.1463-1326.2006.00618.x","article-title":"Topiramate in the treatment of obese subjects with drug-naive type 2 diabetes","volume":"9","author":"Stenl\u00f6f","year":"2007","journal-title":"Diabetes Obes Metab"},{"key":"10.1124\/jpet.116.237057_bib34","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1002\/hipo.20470","article-title":"Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats","volume":"18","author":"Stranahan","year":"2008","journal-title":"Hippocampus"}],"container-title":["The Journal of Pharmacology and Experimental Therapeutics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0022356524194621?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0022356524194621?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1124\/jpet.116.237057","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,19]],"date-time":"2025-02-19T14:50:14Z","timestamp":1739976614000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0022356524194621"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,12]]},"references-count":34,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2016,12]]}},"alternative-id":["S0022356524194621"],"URL":"https:\/\/doi.org\/10.1124\/jpet.116.237057","relation":{},"ISSN":["0022-3565"],"issn-type":[{"value":"0022-3565","type":"print"}],"subject":[],"published":{"date-parts":[[2016,12]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Blood\u2013Brain Barrier Disruption and Neurovascular Unit Dysfunction in Diabetic Mice: Protection with the Mitochondrial Carbonic Anhydrase Inhibitor Topiramate","name":"articletitle","label":"Article Title"},{"value":"The Journal of Pharmacology and Experimental Therapeutics","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1124\/jpet.116.237057","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"U.S. Government work not protected by U.S. copyright","name":"copyright","label":"Copyright"}]}}