{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T16:22:02Z","timestamp":1779294122835,"version":"3.51.4"},"reference-count":80,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,9,24]],"date-time":"2022-09-24T00:00:00Z","timestamp":1663977600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,9,24]],"date-time":"2022-09-24T00:00:00Z","timestamp":1663977600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["UMO-2013\/11\/N\/NZ7\/01643"],"award-info":[{"award-number":["UMO-2013\/11\/N\/NZ7\/01643"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010252","name":"\u015al\u0105ski Uniwersytet Medyczny w Katowicach","doi-asserted-by":"publisher","award":["PCN-1-090\/K\/0\/O"],"award-info":[{"award-number":["PCN-1-090\/K\/0\/O"]}],"id":[{"id":"10.13039\/501100010252","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010252","name":"\u015al\u0105ski Uniwersytet Medyczny w Katowicach","doi-asserted-by":"publisher","award":["PCN-1-090\/K\/0\/O"],"award-info":[{"award-number":["PCN-1-090\/K\/0\/O"]}],"id":[{"id":"10.13039\/501100010252","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Histochem Cell Biol"],"published-print":{"date-parts":[[2023,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The multifaceted nature of subarachnoid hemorrhage (SAH) pathogenesis is poorly understood. To date, no pharmacological agent has been found to be efficacious for the prevention of brain injury when used for acute SAH intervention. This study was undertaken to evaluate the beneficial effects of low-dose neuroprotective agent minocycline on brain microvascular ultrastructures that have not been studied in detail. We studied SAH brain injury using an in\u00a0vivo prechiasmatic subarachnoid hemorrhage rodent model. We analyzed the qualitative and quantitative ultrastructural morphology of capillaries and surrounding neuropil in the rodent brains with SAH and\/or minocycline administration. Here, we report that low-dose minocycline (1\u00a0mg\/kg) displayed protective effects on capillaries and surrounding cells from significant SAH-induced changes. Ultrastructural morphology analysis revealed also that minocycline stopped endothelial cells from abnormal production of vacuoles and vesicles that compromise blood\u2013brain barrier (BBB) transcellular transport. The reported ultrastructural abnormalities as well as neuroprotective effects of minocycline during SAH were not directly mediated by inhibition of MMP-2, MMP-9, or EMMPRIN. However, SAH brain tissue treated with minocycline was protected from development of other morphological features associated with oxidative stress and the presence of immune cells in the perivascular space. These data advance the knowledge on the effect of SAH on brain tissue ultrastructure in an SAH rodent model and the neuroprotective effect of minocycline when administered in low doses.<\/jats:p>","DOI":"10.1007\/s00418-022-02150-9","type":"journal-article","created":{"date-parts":[[2022,9,24]],"date-time":"2022-09-24T16:26:52Z","timestamp":1664036812000},"page":"91-114","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["The protective effect of low-dose minocycline on brain microvascular ultrastructure in a rodent model of subarachnoid hemorrhage"],"prefix":"10.1007","volume":"159","author":[{"given":"Daria","family":"Gendosz de Carrillo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sebastian","family":"Student","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel","family":"Bula","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"\u0141ukasz","family":"Miela\u0144czyk","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ma\u0142gorzata","family":"Burek","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patrick","family":"Meybohm","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Halina","family":"J\u0119drzejowska-Szypu\u0142ka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,9,24]]},"reference":[{"key":"2150_CR1","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.brainresbull.2004.06.006","volume":"64","author":"C Alba","year":"2004","unstructured":"Alba C, Vidal L, D\u00edaz F et\u00a0al (2004) Ultrastructural and quantitative age-related changes in capillaries of the dorsal lateral geniculate nucleus. Brain Res Bull 64:145\u2013153. https:\/\/doi.org\/10.1016\/j.brainresbull.2004.06.006","journal-title":"Brain Res Bull"},{"key":"2150_CR2","doi-asserted-by":"publisher","first-page":"3625","DOI":"10.1177\/0271678X16686595","volume":"37","author":"M Balbi","year":"2017","unstructured":"Balbi M, Koide M, Wellman GC, Plesnila N (2017) Inversion of neurovascular coupling after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab 37:3625\u20133634. https:\/\/doi.org\/10.1177\/0271678X16686595","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR3","doi-asserted-by":"publisher","first-page":"H654","DOI":"10.1152\/ajpheart.00048.2016","volume":"311","author":"O Baum","year":"2016","unstructured":"Baum O, Bigler M (2016) Pericapillary basement membrane thickening in human skeletal muscles. Am J Physiol Hear Circ Physiol 311:H654\u2013H666. https:\/\/doi.org\/10.1152\/ajpheart.00048.2016","journal-title":"Am J Physiol Hear Circ Physiol"},{"key":"2150_CR4","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.1152\/japplphysiol.00594.2015","volume":"119","author":"O Baum","year":"2015","unstructured":"Baum O, G\u00fcbeli J, Frese S et\u00a0al (2015) Angiogenesis-related ultrastructural changes to capillaries in human skeletal muscle in response to endurance exercise. J Appl Physiol 119:1118\u20131126. https:\/\/doi.org\/10.1152\/japplphysiol.00594.2015","journal-title":"J Appl Physiol"},{"key":"2150_CR5","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.it.2006.11.007","volume":"28","author":"I Bechmann","year":"2007","unstructured":"Bechmann I, Galea I, Perry VH (2007) What is the blood\u2013brain barrier (not)? Trends Immunol 28:5\u201311. https:\/\/doi.org\/10.1016\/j.it.2006.11.007","journal-title":"Trends Immunol"},{"key":"2150_CR6","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1186\/2045-8118-8-8","volume":"8","author":"D Bonkowski","year":"2011","unstructured":"Bonkowski D, Katyshev V, Balabanov RD et\u00a0al (2011) The CNS microvascular pericyte: pericyte\u2013astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS 8:8. https:\/\/doi.org\/10.1186\/2045-8118-8-8","journal-title":"Fluids Barriers CNS"},{"key":"2150_CR7","doi-asserted-by":"publisher","DOI":"10.1007\/s12028-022-01511-5","author":"N Care","year":"2022","unstructured":"Care N, Lang KGB, Patsouris V et\u00a0al (2022) Minocycline attenuates microglia\/macrophage phagocytic activity and inhibits SAH-induced neuronal cell death and inflammation. Neurocrit Care. https:\/\/doi.org\/10.1007\/s12028-022-01511-5","journal-title":"Neurocrit Care"},{"key":"2150_CR8","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/j.pneurobio.2013.09.002","volume":"115","author":"S Chen","year":"2014","unstructured":"Chen S, Feng H, Sherchan P et\u00a0al (2014) Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog Neurobiol 115:64\u201391. https:\/\/doi.org\/10.1016\/j.pneurobio.2013.09.002","journal-title":"Prog Neurobiol"},{"key":"2150_CR9","first-page":"455","volume":"52","author":"J Chiang","year":"1968","unstructured":"Chiang J, Kowada M, Ames A et\u00a0al (1968) Cerebral ischemia vascular changes. Am J Pathol 52:455\u2013476","journal-title":"Am J Pathol"},{"key":"2150_CR10","doi-asserted-by":"publisher","first-page":"3993","DOI":"10.1529\/biophysj.103.038422","volume":"86","author":"SV Costes","year":"2004","unstructured":"Costes SV, Daelemans D, Cho EH et\u00a0al (2004) Automatic and quantitative measurement of protein\u2013protein colocalization in live cells. Biophys J 86:3993\u20134003. https:\/\/doi.org\/10.1529\/biophysj.103.038422","journal-title":"Biophys J"},{"key":"2150_CR11","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/0047-6374(92)90083-P","volume":"64","author":"GI De Jong","year":"1992","unstructured":"De Jong GI, Traver J, Luiten PGM (1992) Formation of cerebrovascular anomalies in the ageing rat is delayed by chronic nimodipine application. Mech Ageing Dev 64:255\u2013272. https:\/\/doi.org\/10.1016\/0047-6374(92)90083-P","journal-title":"Mech Ageing Dev"},{"key":"2150_CR12","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1006\/MVRE.2000.2244","volume":"60","author":"P Dore-Duffy","year":"2000","unstructured":"Dore-Duffy P, Owen C, Balabanov R et\u00a0al (2000) Pericyte migration from the vascular wall in response to traumatic brain injury. Microvasc Res 60:55\u201369. https:\/\/doi.org\/10.1006\/MVRE.2000.2244","journal-title":"Microvasc Res"},{"key":"2150_CR13","doi-asserted-by":"publisher","first-page":"292","DOI":"10.3171\/jns.1986.64.2.0292","volume":"64","author":"TA Duff","year":"1986","unstructured":"Duff TA, Scott G, Feilbach JA (1986) Ultrastructural evidence of arterial denervation following experimental subarachnoid hemorrhage. J Neurosurg 64:292\u2013297. https:\/\/doi.org\/10.3171\/jns.1986.64.2.0292","journal-title":"J Neurosurg"},{"key":"2150_CR14","doi-asserted-by":"publisher","first-page":"2909","DOI":"10.1161\/STROKEAHA.115.010351","volume":"46","author":"Y Egashira","year":"2015","unstructured":"Egashira Y, Zhao H, Hua Y et\u00a0al (2015) White matter injury after subarachnoid hemorrhage: role of blood\u2013brain barrier disruption and matrix metalloproteinase-9. Stroke 46:2909\u20132915. https:\/\/doi.org\/10.1161\/STROKEAHA.115.010351","journal-title":"Stroke"},{"key":"2150_CR15","doi-asserted-by":"publisher","first-page":"2283","DOI":"10.1161\/STROKEAHA.110.582601","volume":"41","author":"SC Fagan","year":"2010","unstructured":"Fagan SC, Waller JL, Nichols FT et\u00a0al (2010) Minocycline to improve neurologic outcome in stroke (MINOS): a dose-finding study. Stroke 41:2283\u20132287. https:\/\/doi.org\/10.1161\/STROKEAHA.110.582601","journal-title":"Stroke"},{"key":"2150_CR16","first-page":"1086","volume":"28","author":"RN Frank","year":"1987","unstructured":"Frank RN, Dutta S, Mancini MA (1987) Pericyte coverage is greater in the retinal than in the cerebral capillaries of the rat. Investig Ophthalmol Vis Sci 28:1086\u20131091","journal-title":"Investig Ophthalmol Vis Sci"},{"key":"2150_CR17","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1111\/bph.12139","volume":"169","author":"N Garrido-Mesa","year":"2013","unstructured":"Garrido-Mesa N, Zarzuelo A, G\u00e1lvez J (2013) Minocycline: far beyond an antibiotic. Br J Pharmacol 169:337\u2013352. https:\/\/doi.org\/10.1111\/bph.12139","journal-title":"Br J Pharmacol"},{"key":"2150_CR18","doi-asserted-by":"publisher","first-page":"236","DOI":"10.4161\/cam.28733","volume":"8","author":"A Glentis","year":"2014","unstructured":"Glentis A, Gurchenkov V, Vignjevic DM (2014) Assembly, heterogeneity, and breaching of the basement membranes. Cell Adh Migr 8:236\u2013245. https:\/\/doi.org\/10.4161\/cam.28733","journal-title":"Cell Adh Migr"},{"key":"2150_CR19","doi-asserted-by":"publisher","DOI":"10.1042\/BSR20150256","volume":"36","author":"GD Grass","year":"2015","unstructured":"Grass GD, Toole BP (2015) How, with whom and when: an overview of CD147-mediated regulatory networks influencing matrix metalloproteinase activity. Biosci Rep 36:e00283. https:\/\/doi.org\/10.1042\/BSR20150256","journal-title":"Biosci Rep"},{"key":"2150_CR20","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1177\/0271678X16629976","volume":"37","author":"MJ Haley","year":"2017","unstructured":"Haley MJ, Lawrence CB (2017) The blood\u2013brain barrier after stroke: structural studies and the role of transcytotic vesicles. J Cereb Blood Flow Metab 37:456\u2013470. https:\/\/doi.org\/10.1177\/0271678X16629976","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR21","doi-asserted-by":"publisher","first-page":"2120","DOI":"10.1161\/01.STR.26.11.2120","volume":"26","author":"GF Hamann","year":"1995","unstructured":"Hamann GF, Okada Y, Fitridge R, Del Zoppo GJ (1995) Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 26:2120\u20132126. https:\/\/doi.org\/10.1161\/01.STR.26.11.2120","journal-title":"Stroke"},{"key":"2150_CR22","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1177\/147323001204000328","volume":"40","author":"YZ Hang","year":"2012","unstructured":"Hang YZ, Tu Y, Fu J et\u00a0al (2012) Extracellular matrix metalloproteinase inducer is associated with severity of brain oedema following experimental subarachnoid haemorrhage in rats. J Int Med Res 40:1089\u20131098. https:\/\/doi.org\/10.1177\/147323001204000328","journal-title":"J Int Med Res"},{"key":"2150_CR23","doi-asserted-by":"publisher","DOI":"10.1155\/2009\/329632","volume":"2009","author":"JP Hern\u00e1ndez-Fonseca","year":"2009","unstructured":"Hern\u00e1ndez-Fonseca JP, Rinc\u00f3n J, Pedrea\u00f1ez A et\u00a0al (2009) Structural and ultrastructural analysis of cerebral cortex, cerebellum, and hypothalamus from diabetic rats. Exp Diabetes Res 2009:329632. https:\/\/doi.org\/10.1155\/2009\/329632","journal-title":"Exp Diabetes Res"},{"key":"2150_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0123398","volume":"10","author":"A H\u00f6llig","year":"2015","unstructured":"H\u00f6llig A, Weinandy A, Nolte K et\u00a0al (2015) Experimental subarachnoid hemorrhage in rats: comparison of two endovascular perforation techniques with respect to success rate, confounding pathologies and early hippocampal tissue lesion pattern. PLoS\u00a0One 10:1\u201316. https:\/\/doi.org\/10.1371\/journal.pone.0123398","journal-title":"PLoS\u00a0One"},{"key":"2150_CR25","doi-asserted-by":"publisher","first-page":"19579","DOI":"10.1523\/JNEUROSCI.4318-13.2013","volume":"33","author":"K Jackman","year":"2013","unstructured":"Jackman K, Kahles T, Lane D et\u00a0al (2013) Progranulin deficiency promotes post-ischemic blood\u2013brain barrier disruption. J Neurosci 33:19579\u201319589. https:\/\/doi.org\/10.1523\/JNEUROSCI.4318-13.2013","journal-title":"J Neurosci"},{"key":"2150_CR26","doi-asserted-by":"publisher","first-page":"1138","DOI":"10.4103\/1673-5374.251190","volume":"14","author":"H Kanamaru","year":"2019","unstructured":"Kanamaru H, Suzuki H (2019) Potential therapeutic molecular targets for blood\u2013brain barrier disruption after subarachnoid hemorrhage. Neural Regen Res 14:1138. https:\/\/doi.org\/10.4103\/1673-5374.251190","journal-title":"Neural Regen Res"},{"key":"2150_CR27","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/J.BBR.2008.09.040","volume":"196","author":"H-S Kim","year":"2009","unstructured":"Kim H-S, Suh Y-H (2009) Minocycline and neurodegenerative diseases. Behav Brain Res 196:168\u2013179. https:\/\/doi.org\/10.1016\/J.BBR.2008.09.040","journal-title":"Behav Brain Res"},{"key":"2150_CR28","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1016\/j.neuron.2014.03.003","volume":"82","author":"D Knowland","year":"2014","unstructured":"Knowland D, Arac A, Sekiguchi KJJ et\u00a0al (2014) Stepwise recruitment of transcellular and paracellular pathways underlies blood\u2013brain barrier breakdown in stroke. Neuron 82:603\u2013617. https:\/\/doi.org\/10.1016\/j.neuron.2014.03.003","journal-title":"Neuron"},{"key":"2150_CR29","doi-asserted-by":"publisher","first-page":"2493","DOI":"10.1161\/STROKEAHA.113.000780","volume":"44","author":"E Kohler","year":"2013","unstructured":"Kohler E, Prentice DA, Bates TR et\u00a0al (2013) Intravenous minocycline in acute stroke. Stroke 44:2493\u20132499. https:\/\/doi.org\/10.1161\/STROKEAHA.113.000780","journal-title":"Stroke"},{"key":"2150_CR30","doi-asserted-by":"publisher","first-page":"E1387","DOI":"10.1073\/pnas.1121359109","volume":"109","author":"M Koide","year":"2012","unstructured":"Koide M, Bonev AD, Nelson MT, Wellman GC (2012) Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc Natl Acad Sci U S A 109:E1387\u2013E1395. https:\/\/doi.org\/10.1073\/pnas.1121359109","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2150_CR31","first-page":"167","volume-title":"Acta Neurochirurgica, Supplementum","author":"M Koide","year":"2013","unstructured":"Koide M, Bonev AD, Nelson MT, Wellman GC (2013) Subarachnoid blood converts neurally evoked vasodilation to vasoconstriction in rat brain cortex. Acta Neurochirurgica, Supplementum. Springer Vienna, Vienna, pp 167\u2013171"},{"key":"2150_CR32","doi-asserted-by":"publisher","DOI":"10.1155\/2013\/819340","author":"M Koide","year":"2013","unstructured":"Koide M, Sukhotinsky I, Ayata C, Wellman GC (2013) Subarachnoid hemorrhage, spreading depolarizations and impaired neurovascular coupling. Stroke Res Treat. https:\/\/doi.org\/10.1155\/2013\/819340","journal-title":"Stroke Res Treat"},{"key":"2150_CR33","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1111\/j.1471-4159.2005.03219.x","volume":"94","author":"RL Kraus","year":"2005","unstructured":"Kraus RL, Pasieczny R, Lariosa-Willingham K et\u00a0al (2005) Antioxidant properties of minocycline: neuroprotection in an oxidative stress assay and direct radical-scavenging activity. J Neurochem 94:819\u2013827. https:\/\/doi.org\/10.1111\/j.1471-4159.2005.03219.x","journal-title":"J Neurochem"},{"key":"2150_CR34","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0056419","volume":"8","author":"M Krueger","year":"2013","unstructured":"Krueger M, H\u00e4rtig W, Reichenbach A et\u00a0al (2013) Blood\u2013brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS\u00a0One 8:e56419. https:\/\/doi.org\/10.1371\/journal.pone.0056419","journal-title":"PLoS\u00a0One"},{"key":"2150_CR35","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1038\/jcbfm.2014.199","volume":"35","author":"M Krueger","year":"2015","unstructured":"Krueger M, Bechmann I, Immig K et\u00a0al (2015) Blood\u2013brain barrier breakdown involves four distinct stages of vascular damage in various models of experimental focal cerebral ischemia. J Cereb Blood Flow Metab 35:292\u2013303. https:\/\/doi.org\/10.1038\/jcbfm.2014.199","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR36","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1111\/j.1755-5949.2012.00340.x","volume":"18","author":"WY Liu","year":"2012","unstructured":"Liu WY, Bin WZ, Zhang LC et\u00a0al (2012) Tight junction in blood\u2013brain barrier: an overview of structure, regulation, and regulator substances. CNS Neurosci Ther 18:609\u2013615. https:\/\/doi.org\/10.1111\/j.1755-5949.2012.00340.x","journal-title":"CNS Neurosci Ther"},{"key":"2150_CR37","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method. Methods 25:402\u2013408. https:\/\/doi.org\/10.1006\/meth.2001.1262","journal-title":"Methods"},{"key":"2150_CR38","doi-asserted-by":"publisher","first-page":"439","DOI":"10.3171\/jns.1960.17.3.0439","volume":"17","author":"SA Luse","year":"1960","unstructured":"Luse SA, Harris B (1960) Electron microscopy of the brain in experimental edema. J Neurosurg 17:439\u2013446. https:\/\/doi.org\/10.3171\/jns.1960.17.3.0439","journal-title":"J Neurosurg"},{"key":"2150_CR39","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/S0140-6736(16)30668-7","volume":"389","author":"RL Macdonald","year":"2017","unstructured":"Macdonald RL, Schweizer TA (2017) Spontaneous subarachnoid haemorrhage. Lancet 389:655\u2013666. https:\/\/doi.org\/10.1016\/S0140-6736(16)30668-7","journal-title":"Lancet"},{"key":"2150_CR40","doi-asserted-by":"publisher","first-page":"49","DOI":"10.3171\/jns.1978.48.1.0049","volume":"48","author":"MR Mayberg","year":"1978","unstructured":"Mayberg MR, Wayne Houser O, Sundt TM (1978) Ultrastructural changes in feline arterial endothelium following subarachnoid hemorrhage. J Neurosurg 48:49\u201357. https:\/\/doi.org\/10.3171\/jns.1978.48.1.0049","journal-title":"J Neurosurg"},{"key":"2150_CR41","doi-asserted-by":"publisher","unstructured":"Murakami K, Koide M, Dumont TM et\u00a0al (2011) Subarachnoid hemorrhage induces gliosis and increased expression of the pro-inflammatory cytokine high mobility group box 1 protein. Transl Stroke Res 2:72\u201379. https:\/\/doi.org\/10.1007\/s12975-010-0052-2","DOI":"10.1007\/s12975-010-0052-2"},{"key":"2150_CR42","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1177\/0271678X15608396","volume":"36","author":"PC Nahirney","year":"2016","unstructured":"Nahirney PC, Reeson P, Brown CE (2016) Ultrastructural analysis of blood\u2013brain barrier breakdown in the peri-infarct zone in young adult and aged mice. J Cereb Blood Flow Metab 36:413\u2013425. https:\/\/doi.org\/10.1177\/0271678X15608396","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR43","doi-asserted-by":"publisher","unstructured":"Oka F, Chung DY, Suzuki M, Ayata C (2020) Delayed cerebral ischemia after subarachnoid hemorrhage: experimental-clinical disconnect and the unmet need. Neurocrit Care 32:238\u2013251. https:\/\/doi.org\/10.1007\/s12028-018-0650-5","DOI":"10.1007\/s12028-018-0650-5"},{"key":"2150_CR44","doi-asserted-by":"publisher","first-page":"1825","DOI":"10.1038\/jcbfm.2013.173","volume":"33","author":"L \u00d8stergaard","year":"2013","unstructured":"\u00d8stergaard L, Aamand R, Karabegovic S et\u00a0al (2013) The role of the microcirculation in delayed cerebral ischemia and chronic degenerative changes after subarachnoid hemorrhage. J Cereb Blood Flow Metab 33:1825\u20131837. https:\/\/doi.org\/10.1038\/jcbfm.2013.173","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR45","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1007\/s00401-014-1295-x","volume":"128","author":"I \u00d6zen","year":"2014","unstructured":"\u00d6zen I, Deierborg T, Miharada K et\u00a0al (2014) Brain pericytes acquire a microglial phenotype after stroke. Acta Neuropathol 128:381\u2013396. https:\/\/doi.org\/10.1007\/s00401-014-1295-x","journal-title":"Acta Neuropathol"},{"key":"2150_CR46","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s11010-013-1632-8","volume":"379","author":"A Papadimitropoulou","year":"2013","unstructured":"Papadimitropoulou A, Mamalaki A (2013) The glycosylated IgII extracellular domain of EMMPRIN is implicated in the induction of MMP-2. Mol Cell Biochem 379:107\u2013113. https:\/\/doi.org\/10.1007\/s11010-013-1632-8","journal-title":"Mol Cell Biochem"},{"key":"2150_CR47","doi-asserted-by":"publisher","first-page":"1992","DOI":"10.1007\/s12035-018-1213-7","volume":"56","author":"T Peeyush Kumar","year":"2019","unstructured":"Peeyush Kumar T, McBride DW, Dash PK et\u00a0al (2019) Endothelial cell dysfunction and injury in subarachnoid hemorrhage. Mol Neurobiol 56:1992\u20132006. https:\/\/doi.org\/10.1007\/s12035-018-1213-7","journal-title":"Mol Neurobiol"},{"key":"2150_CR48","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1136\/JNNP.48.3.256","volume":"48","author":"JD Pickard","year":"1985","unstructured":"Pickard JD, Graham DI, Matear E et\u00a0al (1985) Ultrastructure of cerebral arteries following experimental subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 48:256\u2013262. https:\/\/doi.org\/10.1136\/JNNP.48.3.256","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"2150_CR49","doi-asserted-by":"publisher","first-page":"2553","DOI":"10.1097\/01.wnr.0000052320.62862.37","volume":"13","author":"GF Prunell","year":"2002","unstructured":"Prunell GF, Mathiesen T, Svendgaard N-A (2002) A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. NeuroReport 13:2553\u20132556. https:\/\/doi.org\/10.1097\/01.wnr.0000052320.62862.37","journal-title":"NeuroReport"},{"key":"2150_CR50","doi-asserted-by":"publisher","first-page":"1046","DOI":"10.3171\/jns.2005.102.6.1046","volume":"102","author":"GF Prunell","year":"2005","unstructured":"Prunell GF, Svendgaard N-A, Alkass K, Mathiesen T (2005) Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg 102:1046\u20131054. https:\/\/doi.org\/10.3171\/jns.2005.102.6.1046","journal-title":"J Neurosurg"},{"key":"2150_CR51","first-page":"2575","volume":"14","author":"B Raji","year":"2008","unstructured":"Raji B, Dansault A, Vieira V et\u00a0al (2008) Analysis of partner of inscuteable (mPins) expression in the developing mouse eye. Mol Vis 14:2575\u20132598","journal-title":"Mol Vis"},{"key":"2150_CR52","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1083\/jcb.34.1.207","volume":"34","author":"TS Reese","year":"1967","unstructured":"Reese TS, Karnovsky MJ (1967) Fine structural localization of a blood\u2013brain barrier to exogenous peroxidase. J Cell Biol 34:207\u2013217. https:\/\/doi.org\/10.1083\/jcb.34.1.207","journal-title":"J Cell Biol"},{"key":"2150_CR53","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1089\/neu.1995.12.833","volume":"12","author":"GA Rosenberg","year":"1995","unstructured":"Rosenberg GA (1995) Matrix metalloproteinases in brain injury. J Neurotrauma 12:833\u2013842. https:\/\/doi.org\/10.1089\/neu.1995.12.833","journal-title":"J Neurotrauma"},{"key":"2150_CR54","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1016\/j.tcb.2008.08.007","volume":"18","author":"RG Rowe","year":"2008","unstructured":"Rowe RG, Weiss SJ (2008) Breaching the basement membrane: who, when and how? Trends Cell Biol 18:560\u2013574. https:\/\/doi.org\/10.1016\/j.tcb.2008.08.007","journal-title":"Trends Cell Biol"},{"key":"2150_CR55","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.neuroscience.2012.08.002","volume":"224","author":"M Sabri","year":"2012","unstructured":"Sabri M, Ai J, Lakovic K et\u00a0al (2012) Mechanisms of microthrombi formation after experimental subarachnoid hemorrhage. Neuroscience 224:26\u201337. https:\/\/doi.org\/10.1016\/j.neuroscience.2012.08.002","journal-title":"Neuroscience"},{"key":"2150_CR56","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1007\/s00418-021-01992-z","volume":"156","author":"E Salvador","year":"2021","unstructured":"Salvador E, Burek M, L\u00f6hr M et\u00a0al (2021) Senescence and associated blood\u2013brain barrier alterations in vitro. Histochem Cell Biol 156:283\u2013292. https:\/\/doi.org\/10.1007\/s00418-021-01992-z","journal-title":"Histochem Cell Biol"},{"key":"2150_CR57","doi-asserted-by":"publisher","first-page":"1232","DOI":"10.1007\/s11695-017-2992-z","volume":"28","author":"T Sawczyn","year":"2018","unstructured":"Sawczyn T, Zimmermann J, Stygar D et\u00a0al (2018) Ileal transposition (IT) surgery changing the ultrastructure of the transposed segment as well as jejunum. Histomorphometric and electron microscopy analysis. Obes Surg 28:1232\u20131239. https:\/\/doi.org\/10.1007\/s11695-017-2992-z","journal-title":"Obes Surg"},{"key":"2150_CR58","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","volume":"9","author":"CA Schneider","year":"2012","unstructured":"Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671\u2013675. https:\/\/doi.org\/10.1038\/nmeth.2089","journal-title":"Nat Methods"},{"key":"2150_CR59","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/J.BRAINRES.2007.01.034","volume":"1142","author":"K Sch\u00f6ller","year":"2007","unstructured":"Sch\u00f6ller K, Trinkl A, Klopotowski M et\u00a0al (2007) Characterization of microvascular basal lamina damage and blood\u2013brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Res 1142:237\u2013246. https:\/\/doi.org\/10.1016\/J.BRAINRES.2007.01.034","journal-title":"Brain Res"},{"key":"2150_CR60","doi-asserted-by":"publisher","unstructured":"Sehba FA, Mostafa G, Knopman J et\u00a0al (2004) Acute alterations in microvascular basal lamina after subarachnoid hemorrhage. J Neurosurg 101(4):633\u2013640. https:\/\/doi.org\/10.3171\/jns.2004.101.4.0633","DOI":"10.3171\/jns.2004.101.4.0633"},{"key":"2150_CR61","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/978-3-7091-0353-1_9","volume-title":"Early brain injury or cerebral vasospasm","author":"FA Sehba","year":"2011","unstructured":"Sehba FA, Friedrich V (2011) Early micro vascular changes after subarachnoid hemorrhage. Early brain injury or cerebral vasospasm. Springer Vienna, Vienna, pp 49\u201355"},{"key":"2150_CR62","first-page":"199","volume-title":"Acta Neurochirurgica","author":"FA Sehba","year":"2013","unstructured":"Sehba FA, Friedrich V (2013) Cerebral microvasculature is an early target of subarachnoid hemorrhage. Acta Neurochirurgica. Supplementum. Springer Vienna, Vienna, pp 199\u2013205"},{"key":"2150_CR63","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1007\/BF01403606","volume":"100","author":"V Seifert","year":"1989","unstructured":"Seifert V, Stolke D, Reale E (1989) Ultrastructural changes of the basilar artery following experimental subarachnoid haemorrhage. Acta Neurochir (Wien) 100:164\u2013171. https:\/\/doi.org\/10.1007\/BF01403606","journal-title":"Acta Neurochir (Wien)"},{"key":"2150_CR64","doi-asserted-by":"publisher","first-page":"2151","DOI":"10.1002\/j.1460-2075.1990.tb07384.x","volume":"9","author":"H Seulberger","year":"1990","unstructured":"Seulberger H, Lottspeich F, Risau W (1990) The inducible blood\u2013brain barrier specific molecule HT7 is a novel immunoglobulin-like cell surface glycoprotein. EMBO J 9:2151\u20132158","journal-title":"EMBO J"},{"key":"2150_CR65","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/0304-3940(92)90690-9","volume":"140","author":"H Seulberger","year":"1992","unstructured":"Seulberger H, Unger CM, Risau W (1992) HT7, Neurothelin, Basigin, gp42 and OX-47\u2014many names for one developmentally regulated immuno-globulin-like surface glycoprotein on blood\u2013brain barrier endothelium, epithelial tissue barriers and neurons. Neurosci Lett 140:93\u201397. https:\/\/doi.org\/10.1016\/0304-3940(92)90690-9","journal-title":"Neurosci Lett"},{"key":"2150_CR66","doi-asserted-by":"publisher","first-page":"2503","DOI":"10.1089\/neu.2011.1864","volume":"28","author":"P Sherchan","year":"2011","unstructured":"Sherchan P, Lekic T, Suzuki H et\u00a0al (2011) Minocycline improves functional outcomes, memory deficits, and histopathology after endovascular perforation-induced subarachnoid hemorrhage in rats. J Neurotrauma 28:2503\u20132512. https:\/\/doi.org\/10.1089\/neu.2011.1864","journal-title":"J Neurotrauma"},{"key":"2150_CR67","doi-asserted-by":"publisher","first-page":"1140","DOI":"10.1002\/1529-0131(199906)42:6<1140::AID-ANR10>3.0.CO;2-7","volume":"42","author":"GN Smith","year":"1999","unstructured":"Smith GN, Mickler EA, Hasty KA, Brandt KD (1999) Specificity of inhibition of matrix metalloproteinase activity by doxycycline: relationship to structure of the enzyme. Arthritis Rheum 42:1140\u20131146. https:\/\/doi.org\/10.1002\/1529-0131(199906)42:6%3c1140::AID-ANR10%3e3.0.CO;2-7","journal-title":"Arthritis Rheum"},{"key":"2150_CR68","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.jneumeth.2007.08.004","volume":"167","author":"T Sugawara","year":"2008","unstructured":"Sugawara T, Ayer R, Jadhav V, Zhang JH (2008) A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods 167:327\u2013334. https:\/\/doi.org\/10.1016\/j.jneumeth.2007.08.004","journal-title":"J Neurosci Methods"},{"key":"2150_CR69","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s12975-017-0546-2","volume":"9","author":"H Suzuki","year":"2018","unstructured":"Suzuki H, Nakano F (2018) To improve translational research in subarachnoid hemorrhage. Transl Stroke Res 9:1\u20133. https:\/\/doi.org\/10.1007\/s12975-017-0546-2","journal-title":"Transl Stroke Res"},{"key":"2150_CR70","doi-asserted-by":"publisher","first-page":"4043","DOI":"10.1091\/mbc.E04-05-0402","volume":"15","author":"W Tang","year":"2004","unstructured":"Tang W, Chang SB, Hemler ME (2004) Links between CD147 function, glycosylation, and caveolin-1. Mol Biol Cell 15:4043\u20134050. https:\/\/doi.org\/10.1091\/mbc.E04-05-0402","journal-title":"Mol Biol Cell"},{"key":"2150_CR71","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.jns.2007.12.002","volume":"268","author":"SC Thal","year":"2008","unstructured":"Thal SC, Me\u00dfmer K, Schmid-Elsaesser R, Zausinger S (2008) Neurological impairment in rats after subarachnoid hemorrhage\u2014a comparison of functional tests. J Neurol Sci 268:150\u2013159. https:\/\/doi.org\/10.1016\/j.jns.2007.12.002","journal-title":"J Neurol Sci"},{"key":"2150_CR72","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1007\/s12975-014-0323-4","volume":"5","author":"MK Tso","year":"2014","unstructured":"Tso MK, Macdonald RL (2014) Subarachnoid hemorrhage: a review of experimental studies on the microcirculation and the neurovascular unit. Transl Stroke Res 5:174\u2013189. https:\/\/doi.org\/10.1007\/s12975-014-0323-4","journal-title":"Transl Stroke Res"},{"key":"2150_CR73","doi-asserted-by":"publisher","first-page":"3461","DOI":"10.1177\/0271678X16665623","volume":"37","author":"N Turan","year":"2017","unstructured":"Turan N, Miller BA, Heider RA et\u00a0al (2017) Neurobehavioral testing in subarachnoid hemorrhage: a review of methods and current findings in rodents. J Cereb Blood Flow Metab 37:3461\u20133474. https:\/\/doi.org\/10.1177\/0271678X16665623","journal-title":"J Cereb Blood Flow Metab"},{"key":"2150_CR74","doi-asserted-by":"publisher","first-page":"4668","DOI":"10.1091\/mbc.E12-06-0428","volume":"23","author":"RE Tyler","year":"2012","unstructured":"Tyler RE, Pearce MMP, Shaler TA et\u00a0al (2012) Unassembled CD147 is an endogenous endoplasmic reticulum-associated degradation substrate. Mol Biol Cell 23:4668\u20134678. https:\/\/doi.org\/10.1091\/mbc.E12-06-0428","journal-title":"Mol Biol Cell"},{"key":"2150_CR75","doi-asserted-by":"publisher","first-page":"492","DOI":"10.1016\/j.bbadis.2015.10.013","volume":"1862","author":"BJ van Dijk","year":"2015","unstructured":"van Dijk BJ, Vergouwen MDII, Kelfkens MM et\u00a0al (2015) Glial cell response after aneurysmal subarachnoid hemorrhage\u2014functional consequences and clinical implications. Biochim Biophys Acta 1862:492\u2013505. https:\/\/doi.org\/10.1016\/j.bbadis.2015.10.013","journal-title":"Biochim Biophys Acta"},{"key":"2150_CR76","doi-asserted-by":"publisher","DOI":"10.1002\/acn3.492","author":"AK Vellimana","year":"2017","unstructured":"Vellimana AK, Zhou M-L, Singh I et\u00a0al (2017) Minocycline protects against delayed cerebral ischemia after subarachnoid hemorrhage via matrix metalloproteinase-9 inhibition. Ann Clin Transl Neurol. https:\/\/doi.org\/10.1002\/acn3.492","journal-title":"Ann Clin Transl Neurol"},{"key":"2150_CR77","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1007\/s12031-012-9769-6","volume":"48","author":"Z Wang","year":"2012","unstructured":"Wang Z, Meng C-J, Shen X-M et\u00a0al (2012) Potential contribution of hypoxia-inducible factor-1\u03b1, aquaporin-4, and matrix metalloproteinase-9 to blood\u2013brain barrier disruption and brain edema after experimental subarachnoid hemorrhage. J Mol Neurosci 48:273\u2013280. https:\/\/doi.org\/10.1007\/s12031-012-9769-6","journal-title":"J Mol Neurosci"},{"key":"2150_CR78","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1161\/STROKEAHA.120.032397","volume":"52","author":"Z Wang","year":"2021","unstructured":"Wang Z, Chen J, Toyota Y et\u00a0al (2021) Ultra-early cerebral thrombosis formation after experimental subarachnoid hemorrhage detected on T2* magnetic resonance imaging. Stroke 52:1033\u20131042. https:\/\/doi.org\/10.1161\/STROKEAHA.120.032397","journal-title":"Stroke"},{"key":"2150_CR79","doi-asserted-by":"publisher","DOI":"10.1016\/j.mcn.2012.08.012","author":"G Wiera","year":"2013","unstructured":"Wiera G, W\u00f3jtowicz T, Lebida K et\u00a0al (2013) Corrigendum to \u201clong term potentiation affects intracellular metalloproteinases activity in the mossy fiber-CA3 pathway\u201d [molecular and cellular neuroscience 50\/2 (2012) 147-159]. Mol Cell Neurosci. https:\/\/doi.org\/10.1016\/j.mcn.2012.08.012","journal-title":"Mol Cell Neurosci"},{"key":"2150_CR80","doi-asserted-by":"publisher","first-page":"2470","DOI":"10.1177\/0271678X211013595","volume":"41","author":"F Ye","year":"2021","unstructured":"Ye F, Keep RF, Hua Y et\u00a0al (2021) Acute micro-thrombosis after subarachnoid hemorrhage: a new therapeutic target? J Cereb Blood Flow Metab 41:2470\u20132472","journal-title":"J Cereb Blood Flow Metab"}],"container-title":["Histochemistry and Cell Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-022-02150-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00418-022-02150-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-022-02150-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,6]],"date-time":"2023-02-06T02:10:33Z","timestamp":1675649433000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00418-022-02150-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,24]]},"references-count":80,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2023,1]]}},"alternative-id":["2150"],"URL":"https:\/\/doi.org\/10.1007\/s00418-022-02150-9","relation":{},"ISSN":["0948-6143","1432-119X"],"issn-type":[{"value":"0948-6143","type":"print"},{"value":"1432-119X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,24]]},"assertion":[{"value":"31 August 2022","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 September 2022","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare that they have no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"All experimental procedures were approved by the Local Animal Ethics Committee for Experiments on Animals in Katowice (Katowice, Poland) (approval no. 5\/KL\/2012). No human subjects or tissue were utilized in this study.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}}]}}