Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory

Nagy, Vanja; Bozdagi, Ozlem; Matynia, Anna; Balcerzyk, Marcin; Okulski, Pawel; Dzwonek, Joanna; Costa, Rui M.; Silva, Alcino J.; Kaczmarek, Leszek; Huntley, George W.

doi:10.1523/jneurosci.4359-05.2006

Cited by 499Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsProtease and Inhibitor Mechanisms

Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory

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Nagy, Vanja, Bozdagi, Ozlem, Matynia, Anna, Balcerzyk, Marcin, Okulski, Pawel, Dzwonek, Joanna, Costa, Rui M., Silva, Alcino J. +2 more·2006·The Journal of Neuroscience

DOI 10.1523/jneurosci.4359-05.2006PMC PMC4428329

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Abstract

Matrix metalloproteinases (MMPs) are extracellular proteases that have well recognized roles in cell signaling and remodeling in many tissues. In the brain, their activation and function are customarily associated with injury or pathology. Here, we demonstrate a novel role for MMP-9 in hippocampal synaptic physiology, plasticity, and memory. MMP-9 protein levels and proteolytic activity are rapidly increased by stimuli that induce late-phase long-term potentiation (L-LTP) in area CA1. Such regulation requires NMDA receptors and protein synthesis. Blockade of MMP-9 pharmacologically prevents induction of L-LTP selectively; MMP-9 plays no role in, nor is regulated during, other forms of short-term synaptic potentiation or long-lasting synaptic depression. Similarly, in slices from MMP-9 null-mutant mice, hippocampal LTP, but not long-term depression, is impaired in magnitude and duration; adding recombinant active MMP-9 to null-mutant slices restores the magnitude and duration of LTP to wild-type levels. Activated MMP-9 localizes in part to synapses and modulates hippocampal synaptic physiology through integrin receptors, because integrin function-blocking reagents prevent an MMP-9-mediated potentiation of synaptic signal strength. The fundamental importance of MMP-9 function in modulating hippocampal synaptic physiology and plasticity is underscored by behavioral impairments in hippocampal-dependent memory displayed by MMP-9 null-mutant mice. Together, these data reveal new functions for MMPs in synaptic and behavioral plasticity.

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The role of extracellular matrix in cortical plasticity has been previously reported.
“The role of ECM in cortical plasticity has been previously reported (Pizzorusso et al. 2002;Nagy et al. 2006;McRae et al. 2007;Rivera et al. 2010)”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Nagy et al. 2006
MMP9 has been found to be important for the establishment of late long-term potentiation.
“Among the >20 MMPs, MMP9 has been particularly studied and found to be important for the establishment of late long-term potentiation.5, 26”
From Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin (2015) · cites this paper as [26]
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 Nagy et al., 2006
Mice deficient in MMP9 have impaired hippocampal LTP, including at mossy fiber-CA3 synapses, which is restored by adding recombinant active MMP9.
“Mice deficient in MMP9 have impaired hippocampal LTP, including at mossy fiber-CA3 synapses, which is restored by adding recombinant active MMP9 (Nagy et al., 2006; Weira et al., 2013).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Nagy et al., 2006
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 Nagy et al., 2006

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Authors: Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., Costa, R. M., Silva, A. J., Kaczmarek, L., & Huntley, G. W.
Affiliations: Icahn School of Medicine at Mount Sinai (US)
University of California, Los Angeles (US)
Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
Corresponding author: Huntley, George W.
ORCID: Nagy, Vanja
Matynia, Anna
Balcerzyk, Marcin
Dzwonek, Joanna
Costa, Rui M.
Silva, Alcino J.
Kaczmarek, Leszek
Huntley, George W.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2006-02-15
Volume: 26
Issue: 7
Pages: 1923-1934
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.4359-05.2006
PMC: PMC4428329
OpenAlex: W2117308838
Cited by: 499
References: 74
Citations by year: 2026: 15 · 2025: 14 · 2024: 15 · 2023: 24 · 2022: 26 · 2021: 21 · 2020: 24 · 2019: 23 · 2018: 20 · 2017: 27 · 2016: 28 · 2015: 26 · 2014: 36 · 2013: 35 · 2012: 32
FWCI: 10.63
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation (9724504)
National Institutes of Health
U.S. Public Health Service
National Institute of Mental Health (R01MH075783)
National Cancer Institute (R24CA095823)
National Institute of Neurological Disorders and Stroke (NS 34659)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Keywords: MMP-9, hippocampus, CA1, synaptic plasticity, memory, NMDA receptor, protein synthesis, integrins, long-term depression, hippocampal-dependent memory
MeSH terms: Animals, Disease Models, Animal, Hippocampus, Memory, Mice, Inbred C57BL, Neuronal Plasticity, Rats, Sprague-Dawley, Long-Term Potentiation, Pyramidal Cells, Mice, Knockout, Matrix Metalloproteinase 9, Mice, Rats

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Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory

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