In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity
Open accessAbstract
Extracellular proteolysis is an important regulatory nexus for coordinating synaptic functional and structural plasticity, but the identity of such proteases is incompletely understood. Matrix metalloproteinases (MMPs) have well-known, mostly deleterious roles in remodeling after injury or stroke, but their role in nonpathological synaptic plasticity and function in intact adult brains has not been extensively investigated. Here we address the role of MMP-9 in hippocampal synaptic plasticity using both gain- and loss-of-function approaches in urethane-anesthetized adult rats. Acute blockade of MMP-9 proteolytic activity with inhibitors or neutralizing antibodies impairs maintenance, but not induction, of long-term potentiation (LTP) at synapses formed between Schaffer-collaterals and area CA1 dendrites. LTP is associated with significant increases in levels of MMP-9 and proteolytic activity within the potentiated neuropil. By introducing a novel application of gelatin-substrate zymography in vivo, we find that LTP is associated with significantly elevated numbers of gelatinolytic puncta in the potentiated neuropil that codistribute with immunolabeling for MMP-9 and for markers of synapses and dendrites. Such increases in proteolytic activity require NMDA receptor activation. Exposing intact area CA1 neurons to recombinant-active MMP-9 induces a slow synaptic potentiation that mutually occludes, and is occluded by, tetanically evoked potentiation. Taken together, our data reveal novel roles for MMP-mediated proteolysis in regulating nonpathological synaptic function and plasticity in mature hippocampus.
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MMP activity co-localizes with excitatory synapses.
“Consistent with previous studies in the hippocampus (Wilczynski et al., 2008; Bozdagi et al., 2007; Gawlak et al., 2009), we demonstrated that MMP activity co-localizes with excitatory synapses.”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Bozdagi et al., 2007
MMP9 is involved in hippocampal synaptic plasticity.
“One of the most widely studied MMPs in the adult hippocampus, MMP9, is involved in hippocampal synaptic plasticity.”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Bozdagi et al., 2007
Enhanced neural activity in the hippocampus increases the active form of MMP9 into the perisynaptic space.
“Enhanced neural activity in the hippocampus increases the active form of MMP9 into the perisynaptic space (Bozdagi et al., 2007; Nagy et al., 2006; Wiera et al., 2013).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Bozdagi et al., 2007
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- Authors
- Bozdagi, O., Nagy, V., Kwei, K. T., & Huntley, G. W.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2007-07
- Volume
- 98
- Issue
- 1
- Pages
- 334-344
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC4415272
- OpenAlex
- W1981571957
- Cited by
- 182
- References
- 92
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 7 · 2022: 13 · 2021: 9 · 2020: 7 · 2019: 5 · 2018: 7 · 2017: 8 · 2016: 10 · 2015: 11 · 2014: 17 · 2013: 15 · 2012: 14
- FWCI
- 4.36
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH075783, MH075783-01)
- National Institute of Neurological Disorders and Stroke (NS 041687, R01NS041687)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- MMP-9, synaptic plasticity, long-term potentiation, hippocampus, Schaffer collateral-CA1 synapses, NMDA receptor activation, extracellular proteolysis, gelatinase activity, synaptic potentiation, tetanic potentiation
- MeSH terms
- Animals, Dose-Response Relationship, Radiation, Electric Stimulation, Enzyme Inhibitors, Glial Fibrillary Acidic Protein, Hippocampus, Immunoglobulin G, Male, Microtubule-Associated Proteins, Neurons, Synapses, Rats, Sprague-Dawley, Long-Term Potentiation, Matrix Metalloproteinase 9, Vesicular Glutamate Transport Protein 2, Rats, Matrix Metalloproteinase Inhibitors
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