Matrix Metalloproteinase-9 Undergoes Expression and Activation during Dendritic Remodeling in Adult Hippocampus
Open accessAbstract
Neurons of adult brain are able to remodel their synaptic connections in response to various stimuli. Modifications of the peridendritic environment, including the extracellular matrix, are likely to play a role during synapse remodeling. Proteolytic disassembly of ECM is a complex process using the regulated actions of specific extracellular proteinases. One of best-characterized families of matrix-modifying enzymes is the matrix metalloproteinase (MMP) family. Here, we describe changes in the expression and function of two well known MMPs, MMP-9 and MMP-2, in adult rat brain before and after systemic administration of the glutamate receptor agonist kainate. Kainate application results in enhanced synaptic transmission and seizures followed by selective tissue remodeling, primarily in hippocampal dentate gyrus. MMP-9 but not MMP-2 was highly expressed by neurons in normal adult rat brain. MMP-9 protein was localized in neuronal cell bodies and dendrites. Kainate upregulated the level of MMP-9 mRNA and protein within hours after drug administration. This was followed several hours later by MMP-9 enzymatic activation. Within hippocampus, MMP-9 mRNA and activity were increased selectively in dentate gyrus, including its dendritic layer. In addition, MMP-9 mRNA levels decreased in areas undergoing neuronal cell loss. This unique spatiotemporal pattern of MMP-9 expression suggests its involvement in activity-dependent remodeling of dendritic architecture with possible effects on synaptic physiology.
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Heightened MMP activity has been reported in other models of epilepsy, with elevated MMP level associated with epileptiform activity.
“While we suggest a pivotal role for the MMP activity in glioma-associated epilepsy, heightened MMP activity has also been reported in other models of epilepsy46 with elevated MMP level being associated with epileptiform activity47–50.”
From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [49]
The zymography substrate cannot distinguish between the activities of MMP-9 and MMP-2.
“Because MMP-9 has overlapping substrate specificity with MMP-2 (Szklarczyk et al., 2002), the zymography substrate (hereafter called MMP biomarker) cannot distinguish between the activities of these two related metalloproteinases.”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Szklarczyk et al., 2002
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- Authors
- Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R. D. G., & Kaczmarek, L.
- Affiliations
- National Institutes of Health (US)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-02-01
- Volume
- 22
- Issue
- 3
- Pages
- 920-930
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6758472
- OpenAlex
- W2171288469
- Cited by
- 392
- References
- 45
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 7 · 2023: 14 · 2022: 15 · 2021: 11 · 2020: 13 · 2019: 15 · 2018: 17 · 2017: 11 · 2016: 12 · 2015: 19 · 2014: 22 · 2013: 21 · 2012: 20
- FWCI
- 6.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Commission
- Fundacja na rzecz Nauki Polskiej
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- MMP-9, MMP-2, dendritic remodeling, hippocampus, dentate gyrus, extracellular matrix, kainic acid, glutamate receptor agonists, synaptic transmission, seizures, neuronal loss, activity-dependent plasticity, MMP-9 activation
- MeSH terms
- Animals, Dendrites, Enzyme Activation, Extracellular Matrix, Hippocampus, Immunohistochemistry, Kainic Acid, Male, Neuronal Plasticity, Neurons, Organ Specificity, RNA, Messenger, Seizures, Rats, Wistar, In Situ Hybridization, Excitatory Amino Acid Agonists, Reverse Transcriptase Polymerase Chain Reaction, Matrix Metalloproteinase 2, Matrix Metalloproteinase 9, Rats
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