Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia
Open accessAbstract
Deleterious processes of extracellular proteolysis may contribute to the progression of tissue damage after acute brain injury. We recently showed that matrix metalloproteinase-9 (MMP-9) knock-out mice were protected against ischemic and traumatic brain injury. In this study, we examined the mechanisms involved by focusing on relevant MMP-9 substrates in blood-brain barrier, matrix, and white matter. MMP-9 knock-out and wild-type mice were subjected to transient focal ischemia. MMP-9 levels increased after ischemia in wild-type brain, with expression primarily present in vascular endothelium. Western blots showed that the blood-brain barrier-associated protein and MMP-9 substrate zonae occludens-1 was degraded after ischemia, but this was reduced in knock-out mice. There were no detectable changes in another blood-brain barrier-associated protein, occludin. Correspondingly, blood-brain barrier disruption assessed via Evans Blue leakage was significantly attenuated in MMP-9 knock-out mice compared with wild types. In white matter, ischemic degradation of the MMP-9 substrate myelin basic protein was significantly reduced in knock-out mice compared with wild types, whereas there was no degradation of other myelin proteins that are not MMP substrates (proteolipid protein and DM20). There were no detectable changes in the ubiquitous structural protein actin or the extracellular matrix protein laminin. Finally, 24 hr lesion volumes were significantly reduced in knock-out mice compared with wild types. These data demonstrate that the protective effects of MMP-9 gene knock-out after transient focal ischemia may be mediated by reduced proteolytic degradation of critical blood-brain barrier and white matter components.
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In the delayed phase, microglial ROS, especially superoxide radical O2−, increase vascular permeability by stimulating MMP-2/MMP-3/MMP-9 production by microglia, astrocytes and endothelial cells, contributing to hemorrhagic transformation and vasogenic edema.
“In this phase, MMPs are important mediators: microglial ROS, especially superoxide radical O2−, increase vascular permeability also by stimulating MMP-2/MMP-3/MMP-9 production by microglia, astrocytes and ECs (Gottschall and Deb, 1996; Asahi et al., 2001; Rosenberg et al., 2001), contributing to hemorrhagic transformation and vasogenic edema.”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Asahi et al., 2001
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“Despite many studies, the pathomechanism and specific target of MMP-9 in seizure-related neuronal death are unclear, although the role of MMP-9 in other neurodegenerative disorders has been well characterized (Asahi et al., 2001; Kim et al., 2003; Yong, 2005).”
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- Authors
- Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J.-C., Moskowitz, M. A., Fini, M. E., & Lo, E. H.
- Affiliations
- Harvard University (US)
- Tufts University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-10-01
- Volume
- 21
- Issue
- 19
- Pages
- 7724-7732
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762894
- OpenAlex
- W1955736456
- Cited by
- 1,004
- References
- 58
- Citations by year
- 2026: 19 · 2025: 16 · 2024: 33 · 2023: 26 · 2022: 33 · 2021: 36 · 2020: 31 · 2019: 32 · 2018: 42 · 2017: 42 · 2016: 40 · 2015: 55 · 2014: 54 · 2013: 55 · 2012: 46
- FWCI
- 9.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Research to Prevent Blindness
- National Institutes of Health
- National Eye Institute (R01EY012651, R01 EY12651)
- National Institute of Neurological Disorders and Stroke (P50 NS10828, R01-NS38731, R01 NS-40529, R01 NS 37074, R01NS040529, R01NS037074, P50NS010828, R01NS038731)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Epidemiology › Acute Ischemic Stroke Management
- Keywords
- MMP-9, cerebral ischemia, blood-brain barrier disruption, zonula occludens-1, occludin, myelin basic protein, neuroprotection, extracellular matrix, lesion volume
- MeSH terms
- Actins, Animals, Blood-Brain Barrier, Brain, Cell Survival, Ischemic Attack, Transient, Disease Models, Animal, Myelin Basic Protein, Extracellular Matrix, Immunohistochemistry, Laminin, Male, Membrane Proteins, Nerve Fibers, Myelinated, Peptide Hydrolases, Phosphoproteins, Blotting, Western, Mice, Knockout, Matrix Metalloproteinase 9, Mice, Zonula Occludens-1 Protein
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