Stroke-Induced Brain Parenchymal Injury Drives Blood–Brain Barrier Early Leakage Kinetics: A Combined in Vivo/in Vitro Study
The disappointing clinical outcomes of neuroprotectants challenge the relevance of preclinical stroke models and data in defining early cerebrovascular events as potential therapeutic targets. The kinetics of blood–brain barrier (BBB) leakage after reperfusion and the link with parenchymal lesion re...
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creator | Kuntz, Mélanie Mysiorek, Caroline Pétrault, Olivier Pétrault, Maud Uzbekov, Rustem Bordet, Régis Fenart, Laurence Cecchelli, Roméo Bérézowski, Vincent |
description | The disappointing clinical outcomes of neuroprotectants challenge the relevance of preclinical stroke models and data in defining early cerebrovascular events as potential therapeutic targets. The kinetics of blood–brain barrier (BBB) leakage after reperfusion and the link with parenchymal lesion remain debated. By using in vivo and in vitro approaches, we conducted a kinetic analysis of BBB dysfunction during early reperfusion. After 60 minutes of middle cerebral artery occlusion followed by reperfusion times up to 24 hours in mice, a non-invasive magnetic resonance imaging method, through an original sequence of diffusion-weighted imaging, determined brain water mobility in microvascular compartments (D∗) apart from parenchymal compartments (apparent diffusion coefficient). An increase in D∗ found at 4 hours post reperfusion concurred with the onset of both Evans blue/Dextran extravasations and in vitro BBB opening under oxygen-glucose deprivation and reoxygenation (R). The BBB leakage coincided with an emerging cell death in brain tissue as well as in activated glial cells in vitro. The co-culture of BBB endothelial and glial cells evidenced a recovery of endothelium tightness when glial cells were absent or non-injured during R. Preserving the ischemic brain parenchymal cells within 4 hours of reperfusion may improve therapeutic strategies for cerebrovascular protection against stroke. |
doi_str_mv | 10.1038/jcbfm.2013.169 |
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The kinetics of blood–brain barrier (BBB) leakage after reperfusion and the link with parenchymal lesion remain debated. By using in vivo and in vitro approaches, we conducted a kinetic analysis of BBB dysfunction during early reperfusion. After 60 minutes of middle cerebral artery occlusion followed by reperfusion times up to 24 hours in mice, a non-invasive magnetic resonance imaging method, through an original sequence of diffusion-weighted imaging, determined brain water mobility in microvascular compartments (D∗) apart from parenchymal compartments (apparent diffusion coefficient). An increase in D∗ found at 4 hours post reperfusion concurred with the onset of both Evans blue/Dextran extravasations and in vitro BBB opening under oxygen-glucose deprivation and reoxygenation (R). The BBB leakage coincided with an emerging cell death in brain tissue as well as in activated glial cells in vitro. The co-culture of BBB endothelial and glial cells evidenced a recovery of endothelium tightness when glial cells were absent or non-injured during R. Preserving the ischemic brain parenchymal cells within 4 hours of reperfusion may improve therapeutic strategies for cerebrovascular protection against stroke.</description><identifier>ISSN: 0271-678X</identifier><identifier>EISSN: 1559-7016</identifier><identifier>DOI: 10.1038/jcbfm.2013.169</identifier><identifier>PMID: 24084699</identifier><language>eng</language><publisher>London, England: SAGE Publications</publisher><subject>Animals ; Blood-Brain Barrier - metabolism ; Blood-Brain Barrier - pathology ; Blood-Brain Barrier - physiopathology ; Capillary Permeability - physiology ; Cell Death ; Cells, Cultured ; Coculture Techniques ; Disease Models, Animal ; Endothelial Cells - metabolism ; Endothelial Cells - ultrastructure ; Glucose - metabolism ; Kinetics ; Life Sciences ; Magnetic Resonance Imaging ; Male ; Mice ; Mice, Inbred C57BL ; Neuroglia - metabolism ; Neuroglia - ultrastructure ; Original ; Oxygen - metabolism ; Stroke - metabolism ; Stroke - pathology ; Stroke - physiopathology</subject><ispartof>Journal of cerebral blood flow and metabolism, 2014-01, Vol.34 (1), p.95-107</ispartof><rights>2014 ISCBFM</rights><rights>Copyright Nature Publishing Group Jan 2014</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2014 International Society for Cerebral Blood Flow & Metabolism, Inc. 2014 International Society for Cerebral Blood Flow & Metabolism, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-d9670750b5cea8d51bae6374847b6fdd12be15250167a2d1d8598210c82a54b53</citedby><cites>FETCH-LOGICAL-c521t-d9670750b5cea8d51bae6374847b6fdd12be15250167a2d1d8598210c82a54b53</cites><orcidid>0000-0003-2338-8821 ; 0000-0001-9285-0579</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3887349/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3887349/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,21819,27924,27925,43621,43622,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24084699$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-artois.hal.science/hal-02515289$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuntz, Mélanie</creatorcontrib><creatorcontrib>Mysiorek, Caroline</creatorcontrib><creatorcontrib>Pétrault, Olivier</creatorcontrib><creatorcontrib>Pétrault, Maud</creatorcontrib><creatorcontrib>Uzbekov, Rustem</creatorcontrib><creatorcontrib>Bordet, Régis</creatorcontrib><creatorcontrib>Fenart, Laurence</creatorcontrib><creatorcontrib>Cecchelli, Roméo</creatorcontrib><creatorcontrib>Bérézowski, Vincent</creatorcontrib><title>Stroke-Induced Brain Parenchymal Injury Drives Blood–Brain Barrier Early Leakage Kinetics: A Combined in Vivo/in Vitro Study</title><title>Journal of cerebral blood flow and metabolism</title><addtitle>J Cereb Blood Flow Metab</addtitle><description>The disappointing clinical outcomes of neuroprotectants challenge the relevance of preclinical stroke models and data in defining early cerebrovascular events as potential therapeutic targets. The kinetics of blood–brain barrier (BBB) leakage after reperfusion and the link with parenchymal lesion remain debated. By using in vivo and in vitro approaches, we conducted a kinetic analysis of BBB dysfunction during early reperfusion. After 60 minutes of middle cerebral artery occlusion followed by reperfusion times up to 24 hours in mice, a non-invasive magnetic resonance imaging method, through an original sequence of diffusion-weighted imaging, determined brain water mobility in microvascular compartments (D∗) apart from parenchymal compartments (apparent diffusion coefficient). An increase in D∗ found at 4 hours post reperfusion concurred with the onset of both Evans blue/Dextran extravasations and in vitro BBB opening under oxygen-glucose deprivation and reoxygenation (R). The BBB leakage coincided with an emerging cell death in brain tissue as well as in activated glial cells in vitro. The co-culture of BBB endothelial and glial cells evidenced a recovery of endothelium tightness when glial cells were absent or non-injured during R. Preserving the ischemic brain parenchymal cells within 4 hours of reperfusion may improve therapeutic strategies for cerebrovascular protection against stroke.</description><subject>Animals</subject><subject>Blood-Brain Barrier - metabolism</subject><subject>Blood-Brain Barrier - pathology</subject><subject>Blood-Brain Barrier - physiopathology</subject><subject>Capillary Permeability - physiology</subject><subject>Cell Death</subject><subject>Cells, Cultured</subject><subject>Coculture Techniques</subject><subject>Disease Models, Animal</subject><subject>Endothelial Cells - metabolism</subject><subject>Endothelial Cells - ultrastructure</subject><subject>Glucose - metabolism</subject><subject>Kinetics</subject><subject>Life Sciences</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neuroglia - metabolism</subject><subject>Neuroglia - ultrastructure</subject><subject>Original</subject><subject>Oxygen - 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Academic</collection><collection>Neurosciences Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cerebral blood flow and metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuntz, Mélanie</au><au>Mysiorek, Caroline</au><au>Pétrault, Olivier</au><au>Pétrault, Maud</au><au>Uzbekov, Rustem</au><au>Bordet, Régis</au><au>Fenart, Laurence</au><au>Cecchelli, Roméo</au><au>Bérézowski, Vincent</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Stroke-Induced Brain Parenchymal Injury Drives Blood–Brain Barrier Early Leakage Kinetics: A Combined in Vivo/in Vitro Study</atitle><jtitle>Journal of cerebral blood flow and metabolism</jtitle><addtitle>J Cereb Blood Flow Metab</addtitle><date>2014-01-01</date><risdate>2014</risdate><volume>34</volume><issue>1</issue><spage>95</spage><epage>107</epage><pages>95-107</pages><issn>0271-678X</issn><eissn>1559-7016</eissn><abstract>The disappointing clinical outcomes of neuroprotectants challenge the relevance of preclinical stroke models and data in defining early cerebrovascular events as potential therapeutic targets. The kinetics of blood–brain barrier (BBB) leakage after reperfusion and the link with parenchymal lesion remain debated. By using in vivo and in vitro approaches, we conducted a kinetic analysis of BBB dysfunction during early reperfusion. After 60 minutes of middle cerebral artery occlusion followed by reperfusion times up to 24 hours in mice, a non-invasive magnetic resonance imaging method, through an original sequence of diffusion-weighted imaging, determined brain water mobility in microvascular compartments (D∗) apart from parenchymal compartments (apparent diffusion coefficient). An increase in D∗ found at 4 hours post reperfusion concurred with the onset of both Evans blue/Dextran extravasations and in vitro BBB opening under oxygen-glucose deprivation and reoxygenation (R). The BBB leakage coincided with an emerging cell death in brain tissue as well as in activated glial cells in vitro. 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subjects | Animals Blood-Brain Barrier - metabolism Blood-Brain Barrier - pathology Blood-Brain Barrier - physiopathology Capillary Permeability - physiology Cell Death Cells, Cultured Coculture Techniques Disease Models, Animal Endothelial Cells - metabolism Endothelial Cells - ultrastructure Glucose - metabolism Kinetics Life Sciences Magnetic Resonance Imaging Male Mice Mice, Inbred C57BL Neuroglia - metabolism Neuroglia - ultrastructure Original Oxygen - metabolism Stroke - metabolism Stroke - pathology Stroke - physiopathology |
title | Stroke-Induced Brain Parenchymal Injury Drives Blood–Brain Barrier Early Leakage Kinetics: A Combined in Vivo/in Vitro Study |
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