Cited by 1,060Barrier Structure and Function StudiesProtease and Inhibitor MechanismsAcute Ischemic Stroke Management

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Matrix Metalloproteinase-Mediated Disruption of Tight Junction Proteins in Cerebral Vessels is Reversed by Synthetic Matrix Metalloproteinase Inhibitor in Focal Ischemia in Rat

Yang, Yi, Estrada, Eduardo Y, Thompson, Jeffrey F, Liu, Wenlan, Rosenberg, Gary A·2007·Journal of Cerebral Blood Flow & Metabolism

DOI 10.1038/sj.jcbfm.9600375

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Abstract

Matrix metalloproteinases (MMPs) disrupt the blood-brain barrier (BBB) during reperfusion. Occludin and claudins are recently described tight junction proteins (TJPs) that form the BBB. We hypothesized that the opening of the BBB was because of the degradation of TJPs by the MMPs. Spontaneously hypertensive rats had a 90 mins middle cerebral artery occlusion with reperfusion for 2, 3, or 24 h. Matrix metalloproteinases were measured by immunohistochemistry and in situ and gel zymography. Real-time polymerase chain reaction (PCR) measured mRNAs of MMP-2 and -9, furin, membrane-type MMP (MT1-MMP), occludin, and claudin-5. There was opening of the BBB in the piriform cortex after 3 h of reperfusion, and an MMP inhibitor, BB-1101 (30 mg/kg), prevented the opening. At 3 h, in situ zymograms showed gelatinase activity. Zymography and PCR showed greater increases in MMP-2 than in MMP-9. There were increased mRNA and immunohistochemistry for MT1-MMP and furin, which activate MMP-2. Claudin-5 and occludin mRNA expression decreased at 2 h in both hemispheres with fragments of both proteins seen on Western blot by 3 h on the ischemic side; treatment with BB-1101 reversed the degradation of the TJPs. Immunohistochemistry at 3 h showed fragmented TJPs within the endothelial cell clefts. By 24 h, in situ zymography showed gelatinase activity and gel zymography showed elevated levels of MMP-9. Disrupted TJPs previously seen in endothelial cells appeared in the surrounding astrocytes. Our results provide direct evidence that MMPs open the BBB by degrading TJPs and that an MMP inhibitor prevents degradation of the TJPs by MMPs.

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Authors: Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W., & Rosenberg, G. A.
Affiliations: University of New Mexico Health Sciences Center (US)
Corresponding author: Rosenberg, Gary A
ORCID: Yang, Yi
Liu, Wenlan
Rosenberg, Gary A
Venue: Journal of Cerebral Blood Flow & Metabolism
Publisher: SAGE Publications
Published: 2007-04
Volume: 27
Issue: 4
Pages: 697-709
ISSN: 0271-678X (ISSN-L)
1559-7016
DOI: 10.1038/sj.jcbfm.9600375
OpenAlex: W2005675003
Cited by: 1,060
References: 46
Citations by year: 2026: 35 · 2025: 43 · 2024: 37 · 2023: 58 · 2022: 74 · 2021: 67 · 2020: 60 · 2019: 57 · 2018: 55 · 2017: 64 · 2016: 59 · 2015: 65 · 2014: 54 · 2013: 59 · 2012: 56
FWCI: 24.32
Type: journal article
Language: en
Open access: closed
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Neurological Disorders and Stroke (R01NS045847)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Health Sciences › Medicine › Clinical Neurology › Acute Ischemic Stroke Management
Keywords: matrix metalloproteinases, tight junction proteins, blood-brain barrier disruption, focal cerebral ischemia, ischemia-reperfusion injury, occludin, claudin-5, MMP-2, MMP-9, MT1-MMP, furin, middle cerebral artery occlusion, astrocytes, cerebral vasculature
MeSH terms: Animals, Astrocytes, Blood-Brain Barrier, Cerebral Arteries, Brain Ischemia, Cerebral Veins, Evans Blue, Immunohistochemistry, Male, Membrane Proteins, Nerve Tissue Proteins, Protease Inhibitors, Rats, Inbred SHR, RNA, Messenger, Sucrose, Blotting, Western, Reperfusion Injury, Gelatinases, Tight Junctions, Reverse Transcriptase Polymerase Chain Reaction, Infarction, Middle Cerebral Artery, Enzyme Activators, Matrix Metalloproteinase 2, Matrix Metalloproteinases, Endothelial Cells, Furin, Rats, Matrix Metalloproteinase Inhibitors, Claudin-5, Occludin

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Matrix Metalloproteinase-Mediated Disruption of Tight Junction Proteins in Cerebral Vessels is Reversed by Synthetic Matrix Metalloproteinase Inhibitor in Focal Ischemia in Rat

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