{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T05:03:31Z","timestamp":1772168611882,"version":"3.50.1"},"reference-count":110,"publisher":"The Company of Biologists","issue":"9","license":[{"start":{"date-parts":[[2021,2,8]],"date-time":"2021-02-08T00:00:00Z","timestamp":1612742400000},"content-version":"vor","delay-in-days":526,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000849","name":"National Centre for Replacement, Refinement, and Reduction of Animals in Research","doi-asserted-by":"publisher","award":["NC\/P001173\/1"],"award-info":[{"award-number":["NC\/P001173\/1"]}],"id":[{"id":"10.13039\/501100000849","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","award":["105586\/Z\/14\/Z"],"award-info":[{"award-number":["105586\/Z\/14\/Z"]}],"id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000288","name":"Royal Society","doi-asserted-by":"publisher","award":["105586\/Z\/14\/Z"],"award-info":[{"award-number":["105586\/Z\/14\/Z"]}],"id":[{"id":"10.13039\/501100000288","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000274","name":"British Heart Foundation","doi-asserted-by":"publisher","award":["IG\/15\/1\/31328"],"award-info":[{"award-number":["IG\/15\/1\/31328"]}],"id":[{"id":"10.13039\/501100000274","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,9,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Diabetes is associated with dysfunction of the neurovascular unit, although the mechanisms of this are incompletely understood and currently no treatment exists to prevent these negative effects. We previously found that the nitric oxide (NO) donor sodium nitroprusside (SNP) prevents the detrimental effect of glucose on neurovascular coupling in zebrafish. We therefore sought to establish the wider effects of glucose exposure on both the neurovascular unit and on behaviour in zebrafish, and the ability of SNP to prevent these. We incubated 4-days post-fertilisation (dpf) zebrafish embryos in 20\u2005mM glucose or mannitol for 5 days until 9 dpf, with or without 0.1\u2005mM SNP co-treatment for 24\u2005h (8-9 dpf), and quantified vascular NO reactivity, vascular mural cell number, expression of a klf2a reporter, glial fibrillary acidic protein (GFAP) and transient receptor potential cation channel subfamily V member 4 (TRPV4), as well as spontaneous neuronal activation at 9 dpf, all in the optic tectum. We also assessed the effect on light\/dark preference and locomotory characteristics during free-swimming studies. We find that glucose exposure significantly reduced NO reactivity, klf2a reporter expression, vascular mural cell number and TRPV4 expression, while significantly increasing spontaneous neuronal activation and GFAP expression (all in the optic tectum). Furthermore, when we examined larval behaviour, we found that glucose exposure significantly altered light\/dark preference and high and low speed locomotion while in light. Co-treatment with SNP reversed all these molecular and behavioural effects of glucose exposure. Our findings comprehensively describe the negative effects of glucose exposure on the vascular anatomy, molecular phenotype and function of the optic tectum, and on whole-organism behaviour. We also show that SNP or other NO donors may represent a therapeutic strategy to ameliorate the complications of diabetes on the neurovascular unit.<\/jats:p>\n                  <jats:p>This article has an associated First Person interview with the first author of the paper.<\/jats:p>","DOI":"10.1242\/dmm.039867","type":"journal-article","created":{"date-parts":[[2019,9,3]],"date-time":"2019-09-03T11:02:23Z","timestamp":1567508543000},"source":"Crossref","is-referenced-by-count":8,"title":["Sodium nitroprusside prevents the detrimental effects of glucose on the neurovascular unit and behaviour in zebrafish"],"prefix":"10.1242","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8570-0871","authenticated-orcid":false,"given":"Karishma","family":"Chhabria","sequence":"first","affiliation":[{"name":"University of Sheffield 1 Neuroimaging in Cardiovascular Disease (NICAD) Network , , Sheffield, S10 2TN , UK"},{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Avgoustinos","family":"Vouros","sequence":"additional","affiliation":[{"name":"University of Sheffield 4 Department of Computer Science , , Portobello, Sheffield, S1 4DP , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Caroline","family":"Gray","sequence":"additional","affiliation":[{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ryan B.","family":"MacDonald","sequence":"additional","affiliation":[{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhen","family":"Jiang","sequence":"additional","affiliation":[{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2706-316X","authenticated-orcid":false,"given":"Robert Neil","family":"Wilkinson","sequence":"additional","affiliation":[{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Karen","family":"Plant","sequence":"additional","affiliation":[{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eleni","family":"Vasilaki","sequence":"additional","affiliation":[{"name":"University of Sheffield 4 Department of Computer Science , , Portobello, Sheffield, S1 4DP , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6660-9770","authenticated-orcid":false,"given":"Clare","family":"Howarth","sequence":"additional","affiliation":[{"name":"University of Sheffield 1 Neuroimaging in Cardiovascular Disease (NICAD) Network , , Sheffield, S10 2TN , UK"},{"name":"University of Sheffield 5 Department of Psychology , , Cathedral Court, 1 Vicar Lane, Sheffield, S1 2LT , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7458-5481","authenticated-orcid":false,"given":"Timothy J. A.","family":"Chico","sequence":"additional","affiliation":[{"name":"University of Sheffield 1 Neuroimaging in Cardiovascular Disease (NICAD) Network , , Sheffield, S10 2TN , UK"},{"name":"University of Sheffield Medical School 2 Department of Infection, Immunity and Cardiovascular Disease , , Beech Hill Road, Sheffield, S10 2RX , UK"},{"name":"The Bateson Centre, Firth Court, University of Sheffield 3 , Western Bank, Sheffield, S10 2TN , UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2019,9,25]]},"reference":[{"key":"2024061302302637700_DMM039867C1","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1002\/jemt.21029","article-title":"TRPV4 in the sensory organs of adult zebrafish","volume":"75","author":"Amato","year":"2012","journal-title":"Microsc. Res. Tech."},{"key":"2024061302302637700_DMM039867C2","doi-asserted-by":"publisher","first-page":"901","DOI":"10.2337\/diab.37.7.901","article-title":"Effect of intensive insulin therapy on glycemic thresholds for counterregulatory hormone release","volume":"37","author":"Amiel","year":"1988","journal-title":"Diabetes"},{"key":"2024061302302637700_DMM039867C3","doi-asserted-by":"publisher","first-page":"CD003804","DOI":"10.1002\/14651858.CD003804","article-title":"Effect of the treatment of Type II diabetes mellitus on the development of cognitive impairment and dementia","volume":"1","author":"Areosa","year":"2002","journal-title":"Cochrane Database Syst. Rev."},{"key":"2024061302302637700_DMM039867C4","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/j.bbr.2013.05.035","article-title":"Use of the light\/dark test for anxiety in adult and adolescent male rats","volume":"256","author":"Arrant","year":"2013","journal-title":"Behav. Brain Res."},{"key":"2024061302302637700_DMM039867C5","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1038\/nature09613","article-title":"Glial and neuronal control of brain blood flow","volume":"468","author":"Attwell","year":"2010","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C6","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1002\/hbm.22639","article-title":"Neural substrates of approach-avoidance conflict decision-making","volume":"36","author":"Aupperle","year":"2015","journal-title":"Hum. Brain Mapp."},{"key":"2024061302302637700_DMM039867C7","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1007\/s00592-017-1011-0","article-title":"Diabetes mellitus: a risk factor for seizures in the elderly-a population-based study","volume":"54","author":"Baviera","year":"2017","journal-title":"Acta Diabetol."},{"key":"2024061302302637700_DMM039867C8","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1016\/j.neuroscience.2007.06.039","article-title":"Expression and functional characterization of transient receptor potential vanilloid-related channel 4 (TRPV4) in rat cortical astrocytes","volume":"148","author":"Benfenati","year":"2007","journal-title":"Neuroscience"},{"key":"2024061302302637700_DMM039867C9","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/S0959-4388(99)80043-9","article-title":"Clearance of glutamate inside the synapse and beyond","volume":"9","author":"Bergles","year":"1999","journal-title":"Curr. Opin. Neurobiol."},{"key":"2024061302302637700_DMM039867C10","doi-asserted-by":"publisher","DOI":"10.3390\/jdb6010006","article-title":"Imaging neuronal activity in the optic tectum of late stage larval zebrafish","volume":"6","author":"Bergmann","year":"2018","journal-title":"J. Dev. Biol."},{"key":"2024061302302637700_DMM039867C11","doi-asserted-by":"publisher","first-page":"456","DOI":"10.3758\/BF03192800","article-title":"Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods","volume":"38","author":"Blaser","year":"2006","journal-title":"Behav. Res. Methods"},{"key":"2024061302302637700_DMM039867C109","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1016\/j.physbeh.2011.07.029","article-title":"Stimuli affecting zebrafish (Danio rerio) behavior in the light\/dark preference test","volume":"104","author":"Blaser","year":"2011","journal-title":"Physiol. Behav."},{"key":"2024061302302637700_DMM039867C12","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.bbr.2009.11.009","article-title":"Behavioral measures of anxiety in zebrafish (Danio rerio)","volume":"208","author":"Blaser","year":"2010","journal-title":"Behav. Brain Res."},{"key":"2024061302302637700_DMM039867C13","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/S0014-2999(03)01274-3","article-title":"The mouse light\/dark box test","volume":"463","author":"Bourin","year":"2003","journal-title":"Eur. J. Pharmacol."},{"key":"2024061302302637700_DMM039867C14","doi-asserted-by":"publisher","first-page":"1487","DOI":"10.1056\/NEJM198806093182302","article-title":"Plasma glucose concentrations at the onset of hypoglycemic symptoms in patients with poorly controlled diabetes and in nondiabetics","volume":"318","author":"Boyle","year":"1988","journal-title":"N. Engl. J. Med."},{"key":"2024061302302637700_DMM039867C15","doi-asserted-by":"publisher","first-page":"48","DOI":"10.3389\/fendo.2013.00048","article-title":"GABA and glutamate uptake and metabolism in retinal glial (Muller) cells","volume":"4","author":"Bringmann","year":"2013","journal-title":"Front. Endocrinol."},{"key":"2024061302302637700_DMM039867C16","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1016\/S0278-5846(03)00078-2","article-title":"Glutamine synthetase and glutamate dehydrogenase in the prefrontal cortex of patients with schizophrenia","volume":"27","author":"Burbaeva","year":"2003","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"2024061302302637700_DMM039867C17","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.cbpb.2014.03.005","article-title":"Persistent impaired glucose metabolism in a zebrafish hyperglycemia model","volume":"171","author":"Capiotti","year":"2014","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"2024061302302637700_DMM039867C18","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.1001\/jama.1989.03420080075034","article-title":"Glucose control and the renal and retinal complications of insulin-dependent diabetes","volume":"261","author":"Chase","year":"1989","journal-title":"JAMA"},{"key":"2024061302302637700_DMM039867C19","doi-asserted-by":"publisher","first-page":"271678X18810615","DOI":"10.1177\/0271678X18810615","article-title":"The effect of hyperglycemia on neurovascular coupling and cerebrovascular patterning in zebrafish","author":"Chhabria","year":"2018","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"2024061302302637700_DMM039867C20","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1080\/07853890802186921","article-title":"Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis","volume":"41","author":"Chiu","year":"2009","journal-title":"Ann. Med."},{"key":"2024061302302637700_DMM039867C21","doi-asserted-by":"publisher","first-page":"1272","DOI":"10.1016\/j.jdiacomp.2017.04.018","article-title":"Type 2 diabetes is an independent risk factor for dementia conversion in patients with mild cognitive impairment","volume":"31","author":"Ciudin","year":"2017","journal-title":"J. Diabetes Complicat."},{"key":"2024061302302637700_DMM039867C22","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1002\/glia.20068","article-title":"Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS","volume":"48","author":"Coleman","year":"2004","journal-title":"Glia"},{"key":"2024061302302637700_DMM039867C23","doi-asserted-by":"publisher","first-page":"749","DOI":"10.2337\/db13-0519","article-title":"Altered spontaneous brain activity in type 2 diabetes: a resting-state functional MRI study","volume":"63","author":"Cui","year":"2014","journal-title":"Diabetes"},{"key":"2024061302302637700_DMM039867C24","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1136\/bmj.2.6133.325","article-title":"Cerebral blood flow in diabetes mellitus: evidence of abnormal cerebrovascular reactivity","volume":"2","author":"Dandona","year":"1978","journal-title":"Br. Med. J."},{"key":"2024061302302637700_DMM039867C25","doi-asserted-by":"publisher","first-page":"1689","DOI":"10.1182\/blood-2002-01-0046","article-title":"Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2)","volume":"100","author":"Dekker","year":"2002","journal-title":"Blood"},{"key":"2024061302302637700_DMM039867C26","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1016\/S0002-9440(10)63002-7","article-title":"Endothelial KLF2 links local arterial shear stress levels to the expression of vascular tone-regulating genes","volume":"167","author":"Dekker","year":"2005","journal-title":"Am. J. Pathol."},{"key":"2024061302302637700_DMM039867C27","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1016\/S0959-437X(00)00074-5","article-title":"Zebrafish: a model system for the study of human disease","volume":"10","author":"Dooley","year":"2000","journal-title":"Curr. Opin. Genet. Dev."},{"key":"2024061302302637700_DMM039867C28","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1172\/JCI11235","article-title":"Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site","volume":"108","author":"Du","year":"2001","journal-title":"J. Clin. Invest."},{"key":"2024061302302637700_DMM039867C29","doi-asserted-by":"publisher","first-page":"6157","DOI":"10.1073\/pnas.1216514110","article-title":"TRPV4 channels stimulate Ca2+-induced Ca2+ release in astrocytic endfeet and amplify neurovascular coupling responses","volume":"110","author":"Dunn","year":"2013","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024061302302637700_DMM039867C30","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.bbr.2009.06.022","article-title":"Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish","volume":"205","author":"Egan","year":"2009","journal-title":"Behav. Brain Res."},{"key":"2024061302302637700_DMM039867C31","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1097\/FJC.0b013e318279ba42","article-title":"TRPV4 and the regulation of vascular tone","volume":"61","author":"Filosa","year":"2013","journal-title":"J. Cardiovasc. Pharmacol."},{"key":"2024061302302637700_DMM039867C32","first-page":"999","article-title":"Pericyte coverage of retinal and cerebral capillaries","volume":"31","author":"Frank","year":"1990","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"2024061302302637700_DMM039867C33","doi-asserted-by":"publisher","first-page":"133","DOI":"10.3858\/emm.2009.41.3.016","article-title":"Tie2 is tied at the cell-cell contacts and to extracellular matrix by angiopoietin-1","volume":"41","author":"Fukuhara","year":"2009","journal-title":"Exp. Mol. Med."},{"key":"2024061302302637700_DMM039867C34","doi-asserted-by":"publisher","first-page":"630","DOI":"10.1161\/ATVBAHA.107.161521","article-title":"Endothelial-mural cell signaling in vascular development and angiogenesis","volume":"29","author":"Gaengel","year":"2009","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"2024061302302637700_DMM039867C35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00417-016-3548-y","article-title":"The neurovascular unit and the pathophysiologic basis of diabetic retinopathy","volume":"255","author":"Gardner","year":"2017","journal-title":"Graefe's Arch. Clin. Exp. Ophthalmol."},{"key":"2024061302302637700_DMM039867C36","doi-asserted-by":"publisher","first-page":"14562","DOI":"10.1038\/srep14562","article-title":"Detailed classification of swimming paths in the Morris Water Maze: multiple strategies within one trial","volume":"5","author":"Gehring","year":"2015","journal-title":"Sci. Rep."},{"key":"2024061302302637700_DMM039867C37","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1007\/s00441-003-0745-x","article-title":"Endothelial-pericyte interactions in angiogenesis","volume":"314","author":"Gerhardt","year":"2003","journal-title":"Cell Tissue Res."},{"key":"2024061302302637700_DMM039867C38","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1136\/gut.2010.220913","article-title":"Endothelial expression of transcription factor Kruppel-like factor 2 and its vasoprotective target genes in the normal and cirrhotic rat liver","volume":"60","author":"Gracia-Sancho","year":"2011","journal-title":"Gut"},{"key":"2024061302302637700_DMM039867C39","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1113\/jphysiol.2006.121111","article-title":"Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice","volume":"578","author":"Grant","year":"2007","journal-title":"J. Physiol."},{"key":"2024061302302637700_DMM039867C40","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/S0165-0270(03)00187-0","article-title":"Automatic recognition of explorative strategies in the Morris water maze","volume":"130","author":"Graziano","year":"2003","journal-title":"J. Neurosci. Methods"},{"key":"2024061302302637700_DMM039867C41","doi-asserted-by":"publisher","first-page":"1253","DOI":"10.1016\/j.numecd.2018.07.008","article-title":"Brain imaging correlates of mild cognitive impairment and early dementia in patients with type 2 diabetes mellitus","volume":"28","author":"Groeneveld","year":"2018","journal-title":"Nutr. Metab. Cardiovasc. Dis."},{"key":"2024061302302637700_DMM039867C42","doi-asserted-by":"publisher","first-page":"E938","DOI":"10.3390\/ijms19040938","article-title":"The role of endothelial Ca(2+) signaling in neurovascular coupling: a view from the lumen","volume":"19","author":"Guerra","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"2024061302302637700_DMM039867C43","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1038\/nature13165","article-title":"Capillary pericytes regulate cerebral blood flow in health and disease","volume":"508","author":"Hall","year":"2014","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C44","doi-asserted-by":"publisher","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":"2024061302302637700_DMM039867C45","doi-asserted-by":"publisher","first-page":"4001","DOI":"10.1242\/dev.039990","article-title":"Vegfc\/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries","volume":"136","author":"Hogan","year":"2009","journal-title":"Development"},{"key":"2024061302302637700_DMM039867C46","first-page":"1","article-title":"Alteration of the GABAergic neuronal system of the retina and superior colliculus in streptozotocin-induced diabetic rat","volume":"44","author":"Honda","year":"1998","journal-title":"Kobe J. Med. Sci."},{"key":"2024061302302637700_DMM039867C47","doi-asserted-by":"publisher","first-page":"9265","DOI":"10.1073\/pnas.84.24.9265","article-title":"Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide","volume":"84","author":"Ignarro","year":"1987","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2024061302302637700_DMM039867C48","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1016\/j.bbi.2015.10.013","article-title":"Unraveling cognitive traits using the Morris water maze unbiased strategy classification (MUST-C) algorithm","volume":"52","author":"Illouz","year":"2016","journal-title":"Brain Behav. Immun."},{"key":"2024061302302637700_DMM039867C110","doi-asserted-by":"publisher","first-page":"e19713","DOI":"10.1371\/journal.pone.0019713","article-title":"One for all \u2013 a highly efficient and versatile method for fluorescent immunostaining in fish embryos","volume":"6","author":"Inoue","year":"2011","journal-title":"PLoS ONE"},{"key":"2024061302302637700_DMM039867C49","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1038\/325253a0","article-title":"Astrocytes induce blood-brain barrier properties in endothelial cells","volume":"325","author":"Janzer","year":"1987","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C50","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/S0140-6736(94)92757-X","article-title":"Effect of blood pressure and diabetes on stroke in progression","volume":"344","author":"J\u00f8rgensen","year":"1994","journal-title":"Lancet"},{"key":"2024061302302637700_DMM039867C111","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1089\/zeb.2012.0861","article-title":"Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond","volume":"10","author":"Kalueff","year":"2013","journal-title":"Zebrafish"},{"key":"2024061302302637700_DMM039867C51","doi-asserted-by":"publisher","first-page":"1577","DOI":"10.1111\/j.1476-5381.2010.00872.x","article-title":"Animal research: reporting in vivo experiments: the ARRIVE guidelines","volume":"160","author":"Kilkenny","year":"2010","journal-title":"Br. J. Pharmacol."},{"key":"2024061302302637700_DMM039867C52","doi-asserted-by":"publisher","first-page":"14241","DOI":"10.1038\/srep14241","article-title":"Diabetic pdx1-mutant zebrafish show conserved responses to nutrient overload and anti-glycemic treatment","volume":"5","author":"Kimmel","year":"2015","journal-title":"Sci. Rep."},{"key":"2024061302302637700_DMM039867C53","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.physbeh.2014.05.006","article-title":"Assessment of mouse anxiety-like behavior in the light-dark box and open-field arena: role of equipment and procedure","volume":"133","author":"Kulesskaya","year":"2014","journal-title":"Physiol. Behav."},{"key":"2024061302302637700_DMM039867C54","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1089\/zeb.2016.1415","article-title":"Comparative analyses of zebrafish anxiety-like behavior using conflict-based novelty tests","volume":"14","author":"Kysil","year":"2017","journal-title":"Zebrafish"},{"key":"2024061302302637700_DMM039867C55","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.aquaculture.2007.04.077","article-title":"The husbandry of zebrafish (Danio rerio): a review","volume":"269","author":"Lawrence","year":"2007","journal-title":"Aquaculture"},{"key":"2024061302302637700_DMM039867C56","doi-asserted-by":"publisher","first-page":"1861","DOI":"10.1016\/S0002-9440(10)62495-9","article-title":"Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts","volume":"166","author":"Lee","year":"2005","journal-title":"Am. J. Pathol."},{"key":"2024061302302637700_DMM039867C57","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.physbeh.2006.08.026","article-title":"Anxiolytic effects of nicotine in zebrafish","volume":"90","author":"Levin","year":"2007","journal-title":"Physiol. Behav."},{"key":"2024061302302637700_DMM039867C58","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1006\/exer.2002.1170","article-title":"Early retinal damage in experimental diabetes: electroretinographical and morphological observations","volume":"74","author":"Li","year":"2002","journal-title":"Exp. Eye Res."},{"key":"2024061302302637700_DMM039867C59","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1038\/nrg2091","article-title":"Animal models of human disease: zebrafish swim into view","volume":"8","author":"Lieschke","year":"2007","journal-title":"Nat. Rev. Genet."},{"key":"2024061302302637700_DMM039867C60","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1006\/exer.2000.0840","article-title":"Diabetes reduces glutamate oxidation and glutamine synthesis in the retina","volume":"70","author":"Lieth","year":"2000","journal-title":"Exp. Eye Res."},{"key":"2024061302302637700_DMM039867C61","doi-asserted-by":"publisher","first-page":"e48","DOI":"10.1161\/01.RES.0000159707.05637.a1","article-title":"Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function","volume":"96","author":"Lin","year":"2005","journal-title":"Circ. Res."},{"key":"2024061302302637700_DMM039867C62","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1159\/000064928","article-title":"Diabetes mellitus and the risk of dementia, Alzheimer's disease and vascular cognitive impairment in the canadian study of health and aging","volume":"14","author":"MacKnight","year":"2002","journal-title":"Dement Geriatr. Cogn. Disord."},{"key":"2024061302302637700_DMM039867C63","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1016\/j.modgep.2006.10.011","article-title":"Dynamic expression of the osmosensory channel trpv4 in multiple developing organs in zebrafish","volume":"7","author":"Mangos","year":"2007","journal-title":"Gene Expression Patterns"},{"key":"2024061302302637700_DMM039867C64","doi-asserted-by":"publisher","first-page":"H1390","DOI":"10.1152\/ajpheart.01006.2006","article-title":"PLA2 and TRPV4 channels regulate endothelial calcium in cerebral arteries","volume":"292","author":"Marrelli","year":"2007","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"2024061302302637700_DMM039867C65","doi-asserted-by":"publisher","first-page":"458","DOI":"10.1016\/S1575-0922(09)73314-5","article-title":"[Occipital seizures with electroencephalographic alterations as the initial manifestation of diabetes mellitus]","volume":"56","author":"Martinez","year":"2009","journal-title":"Endocrinologia y nutricion: organo de la Sociedad Espanola de Endocrinologia y Nutricion"},{"key":"2024061302302637700_DMM039867C66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jchemneu.2012.10.001","article-title":"\u201cLimbic associative\u201d and \u201cautonomic\u201d amygdala in teleosts: a review of the evidence","volume":"48-49","author":"Maximino","year":"2013","journal-title":"J. Chem. Neuroanat."},{"key":"2024061302302637700_DMM039867C68","doi-asserted-by":"publisher","first-page":"69","DOI":"10.2337\/diacare.21.1.69","article-title":"Impact of diabetes on mortality after the first myocardial infarction. The FINMONICA myocardial infarction register study group","volume":"21","author":"Miettinen","year":"1998","journal-title":"Diabetes Care"},{"key":"2024061302302637700_DMM039867C69","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1253\/circj.CJ-11-0121","article-title":"Neurovascular coupling in cognitive impairment associated with diabetes mellitus","volume":"75","author":"Mogi","year":"2011","journal-title":"Circ. J."},{"key":"2024061302302637700_DMM039867C70","doi-asserted-by":"publisher","first-page":"e0128359","DOI":"10.1371\/journal.pone.0128359","article-title":"Hyperglycemia and diabetes downregulate the functional expression of TRPV4 channels in retinal microvascular endothelium","volume":"10","author":"Monaghan","year":"2015","journal-title":"PLoS ONE"},{"key":"2024061302302637700_DMM039867C71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1741-7007-8-126","article-title":"Focusing on optic tectum circuitry through the lens of genetics","volume":"8","author":"Nevin","year":"2010","journal-title":"BMC Biol."},{"key":"2024061302302637700_DMM039867C72","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/0166-2236(96)10040-0","article-title":"The M\u00fcller cell: a functional element of the retina","volume":"19","author":"Newman","year":"1996","journal-title":"Trends Neurosci."},{"key":"2024061302302637700_DMM039867C73","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1089\/zeb.2011.0690","article-title":"Fighting zebrafish: characterization of aggressive behavior and winner-loser effects","volume":"8","author":"Oliveira","year":"2011","journal-title":"Zebrafish"},{"key":"2024061302302637700_DMM039867C74","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.jdiacomp.2012.03.007","article-title":"Evaluation of metabolite changes in visual cortex in diabetic retinopathy by MR-spectroscopy","volume":"26","author":"Ozsoy","year":"2012","journal-title":"J. Diabetes Complicat."},{"key":"2024061302302637700_DMM039867C75","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/327524a0","article-title":"Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor","volume":"27","author":"Palmer","year":"1987","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C76","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1038\/35103567","article-title":"The art and design of genetic screens: zebrafish","volume":"2","author":"Patton","year":"2001","journal-title":"Nat. Rev. Genet."},{"key":"2024061302302637700_DMM039867C77","doi-asserted-by":"publisher","first-page":"700","DOI":"10.1038\/nature05193","article-title":"Bidirectional control of CNS capillary diameter by pericytes","volume":"443","author":"Peppiatt","year":"2006","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C78","doi-asserted-by":"publisher","first-page":"2495","DOI":"10.2337\/db08-0325","article-title":"Pericyte migration: a novel mechanism of pericyte loss in experimental diabetic retinopathy","volume":"57","author":"Pfister","year":"2008","journal-title":"Diabetes"},{"key":"2024061302302637700_DMM039867C79","doi-asserted-by":"publisher","first-page":"1047","DOI":"10.1161\/01.HYP.31.5.1047","article-title":"Review of alterations in endothelial nitric oxide production in diabetes: protective role of arginine on endothelial dysfunction","volume":"31","author":"Pieper","year":"1998","journal-title":"Hypertension"},{"key":"2024061302302637700_DMM039867C80","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1016\/j.mod.2006.11.005","article-title":"Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase","volume":"124","author":"Pisharath","year":"2007","journal-title":"Mech. Dev."},{"key":"2024061302302637700_DMM039867C81","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1002\/glia.1104","article-title":"Glial cell influence on the human blood-brain barrier","volume":"36","author":"Prat","year":"2001","journal-title":"Glia"},{"key":"2024061302302637700_DMM039867C82","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.bbr.2011.11.041","article-title":"On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae","volume":"228","author":"Richendrfer","year":"2012","journal-title":"Behav. Brain Res."},{"key":"2024061302302637700_DMM039867C83","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1113\/jphysiol.1890.sp000321","article-title":"On the regulation of the blood-supply of the brain","volume":"11","author":"Roy","year":"1890","journal-title":"J. Physiol."},{"key":"2024061302302637700_DMM039867C84","first-page":"1971","article-title":"Glial reactivity, an early feature of diabetic retinopathy","volume":"41","author":"Rungger-Brandle","year":"2000","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"2024061302302637700_DMM039867C85","doi-asserted-by":"publisher","first-page":"2932","DOI":"10.1038\/ncomms3932","article-title":"Pericyte loss influences Alzheimer-like neurodegeneration in mice","volume":"4","author":"Sagare","year":"2013","journal-title":"Nat. Commun."},{"key":"2024061302302637700_DMM039867C86","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1006\/mvre.2001.2343","article-title":"Nitric oxide\/cGMP-induced inhibition of calcium and chloride currents in retinal pericytes","volume":"62","author":"Sakagami","year":"2001","journal-title":"Microvasc. Res."},{"key":"2024061302302637700_DMM039867C87","doi-asserted-by":"publisher","first-page":"13","DOI":"10.3389\/neuro.04.013.2009","article-title":"The cellular architecture of the larval zebrafish tectum, as revealed by gal4 enhancer trap lines","volume":"3","author":"Scott","year":"2009","journal-title":"Front. Neural Circuits"},{"key":"2024061302302637700_DMM039867C88","doi-asserted-by":"publisher","first-page":"S2","DOI":"10.1038\/485S2a","article-title":"Diabetes in numbers","volume":"485","author":"Scully","year":"2012","journal-title":"Nature"},{"key":"2024061302302637700_DMM039867C89","doi-asserted-by":"publisher","first-page":"1305","DOI":"10.1084\/jem.20031132","article-title":"KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation","volume":"199","author":"SenBanerjee","year":"2004","journal-title":"J. Exp. Med."},{"key":"2024061302302637700_DMM039867C90","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1007\/s00592-017-0970-5","article-title":"Cognitive impairment and dementia: a new emerging complication of type 2 diabetes-The diabetologist's perspective","volume":"54","author":"Sim\u00f3","year":"2017","journal-title":"Acta Diabetol."},{"key":"2024061302302637700_DMM039867C91","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.2337\/diabetes.49.6.1006","article-title":"Effects of DL-alpha-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy","volume":"49","author":"Stevens","year":"2000","journal-title":"Diabetes"},{"key":"2024061302302637700_DMM039867C92","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1046\/j.1464-5491.1999.00027.x","article-title":"Type 2 diabetes mellitus, cognitive impairment and dementia","volume":"16","author":"Stewart","year":"1999","journal-title":"Diabet. Med."},{"key":"2024061302302637700_DMM039867C93","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1136\/bmj.321.7258.405","article-title":"Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study","volume":"321","author":"Stratton","year":"2000","journal-title":"BMJ"},{"key":"2024061302302637700_DMM039867C94","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.phrs.2013.09.005","article-title":"TRPV4 channel activation leads to endothelium-dependent relaxation mediated by nitric oxide and endothelium-derived hyperpolarizing factor in rat pulmonary artery","volume":"78","author":"Sukumaran","year":"2013","journal-title":"Pharmacol. Res."},{"key":"2024061302302637700_DMM039867C95","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.cbpa.2013.05.027","article-title":"How ubiquitous is endothelial NOS?","volume":"166","author":"Syeda","year":"2013","journal-title":"Comp. Biochem. Phys. A"},{"key":"2024061302302637700_DMM039867C96","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1038\/nn1623","article-title":"Astrocyte-mediated control of cerebral blood flow","volume":"9","author":"Takano","year":"2006","journal-title":"Nat. Neurosci."},{"key":"2024061302302637700_DMM039867C97","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1007\/BF00703132","article-title":"Pericyte degeneration and acellular capillaries are increased in the feet of human diabetic patients","volume":"28","author":"Tilton","year":"1985","journal-title":"Diabetologia"},{"key":"2024061302302637700_DMM039867C98","doi-asserted-by":"publisher","first-page":"H1837","DOI":"10.1152\/ajpheart.00463.2015","article-title":"Purinergic glio-endothelial coupling during neuronal activity: role of P2Y1 receptors and eNOS in functional hyperemia in the mouse somatosensory cortex","volume":"309","author":"Toth","year":"2015","journal-title":"Am. J Physiol. Heart Circ. Physiol."},{"key":"2024061302302637700_DMM039867C99","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1038\/nm0910-959","article-title":"Pericyte constriction after stroke: the jury is still out","volume":"16","author":"Vates","year":"2010","journal-title":"Nat. Med."},{"key":"2024061302302637700_DMM039867C100","doi-asserted-by":"publisher","first-page":"15089","DOI":"10.1038\/s41598-018-33456-1","article-title":"A generalised framework for detailed classification of swimming paths inside the Morris Water Maze","volume":"8","author":"Vouros","year":"2018","journal-title":"Sci. Rep."},{"key":"2024061302302637700_DMM039867C101","doi-asserted-by":"publisher","first-page":"908","DOI":"10.1161\/01.RES.0000187474.47805.30","article-title":"Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium","volume":"97","author":"Vriens","year":"2005","journal-title":"Circ. Res."},{"key":"2024061302302637700_DMM039867C102","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1016\/0735-1097(95)00522-6","article-title":"Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus","volume":"27","author":"Williams","year":"1996","journal-title":"J. Am. Coll. Cardiol."},{"key":"2024061302302637700_DMM039867C103","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1111\/j.1469-445X.2000.02095.x","article-title":"Dissecting the behaviour of transgenic mice: is it the mutation, the genetic background, or the environment?","volume":"85","author":"Wolfer","year":"2000","journal-title":"Exp. Physiol."},{"key":"2024061302302637700_DMM039867C104","doi-asserted-by":"publisher","first-page":"3942","DOI":"10.1074\/jbc.M707882200","article-title":"KLF2 transcription factor modulates blood vessel maturation through smooth muscle cell migration","volume":"283","author":"Wu","year":"2008","journal-title":"J. Biol. Chem."},{"key":"2024061302302637700_DMM039867C105","doi-asserted-by":"publisher","first-page":"966","DOI":"10.1161\/CIRCRESAHA.107.168724","article-title":"Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4","volume":"102","author":"Yin","year":"2008","journal-title":"Circ. Res."},{"key":"2024061302302637700_DMM039867C106","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.diabres.2010.01.026","article-title":"Global healthcare expenditure on diabetes for 2010 and 2030","volume":"87","author":"Zhang","year":"2010","journal-title":"Diabetes Res. Clin. Pract."},{"key":"2024061302302637700_DMM039867C107","doi-asserted-by":"publisher","first-page":"1370","DOI":"10.1038\/nm1210-1370","article-title":"Neurodegeneration and the neurovascular unit","volume":"16","author":"Zlokovic","year":"2010","journal-title":"Nat. Med."},{"key":"2024061302302637700_DMM039867C108","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1038\/nn980","article-title":"Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation","volume":"6","author":"Zonta","year":"2003","journal-title":"Nat. Neurosci."}],"container-title":["Disease Models &amp; Mechanisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1242\/dmm.039867","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.039867\/3484240\/dmm039867.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.039867\/2065597\/dmm_039867v1.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.039867\/3484240\/dmm039867.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,12]],"date-time":"2024-06-12T22:30:46Z","timestamp":1718231446000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dmm\/article\/12\/9\/dmm039867\/224218\/Sodium-nitroprusside-prevents-the-detrimental"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,1]]},"references-count":110,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2019,9,1]]}},"URL":"https:\/\/doi.org\/10.1242\/dmm.039867","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/576942","asserted-by":"object"}]},"ISSN":["1754-8411","1754-8403"],"issn-type":[{"value":"1754-8411","type":"electronic"},{"value":"1754-8403","type":"print"}],"subject":[],"published":{"date-parts":[[2019,9,1]]},"article-number":"dmm039867"}}