The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory

Nagy, Vanja; Bozdagi, Ozlem; Huntley, George W.

doi:10.1101/lm.678307

PreprintCited by 107Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchProtease and Inhibitor Mechanisms

The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory

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Nagy, Vanja, Bozdagi, Ozlem, Huntley, George W.·2007·Learning & Memory

DOI 10.1101/lm.678307PMC PMC2044557

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Abstract

Matrix metalloproteinases (MMPs) are a family of extracellularly acting proteolytic enzymes with well-recognized roles in plasticity and remodeling of synaptic circuits during brain development and following brain injury. However, it is now becoming increasingly apparent that MMPs also function in normal, nonpathological synaptic plasticity of the kind that may underlie learning and memory. Here, we extend this idea by investigating the role and regulation of MMP-9 in an inhibitory avoidance (IA) learning and memory task. We demonstrate that following IA training, protein levels and proteolytic activity of MMP-9 become elevated in hippocampus by 6 h, peak at 12-24 h, then decline to baseline values by approximately 72 h. When MMP function is abrogated by intrahippocampal infusion of a potent gelatinase (MMP-2 and MMP-9) inhibitor 3.5 h following IA training, a time prior to the onset of training-induced elevation in levels, IA memory retention is significantly diminished when tested 1-3 d later. Animals impaired at 3 d exhibit robust IA memory when retrained, suggesting that such impairment is not likely attributed to toxic or other deleterious effects that permanently disrupt hippocampal function. In anesthetized adult rats, the effective distance over which synaptic plasticity is impaired by a single intrahippocampal infusion of the MMP inhibitor of the kind that blocks IA memory is approximately 1200 microm. Taken together, these data suggest that IA training induces a slowly emerging, but subsequently protracted period of MMP-mediated proteolysis critical for enabling long-lasting synaptic modification that underlies long-term memory consolidation.

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Disrupting MMP3 and MMP9 activity in hippocampus impairs spatial memory and avoidance learning.
“Similar disruption of MMP3 and MMP9 activity in the hippocampus results in disruption of spatial memory and avoidance learning (Nagy et al., 2007; Wright et al., 2007).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Nagy et al., 2007

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Glutaminase and MMP-9 Downregulation in Cortex and Hippocampus of LPA1 Receptor Null Mice Correlate with Altered Dendritic Spine Plasticity
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Sleep and Memory Consolidation Dysfunction in Psychiatric Disorders: Evidence for the Involvement of Extracellular Matrix Molecules
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Prospective cohort study reveals MMP-9, a neuroplasticity regulator, as a prediction marker of cochlear implantation outcome in prelingual deafness treatment
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Extracellular matrix metalloproteinase-9 (MMP-9) is required in female mice for 17β-estradiol enhancement of hippocampal memory consolidation
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Circadian Rhythms of Perineuronal Net CompositionPreprint
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doi:10.1155/2007/73813 Research Article Inhibition of Hippocampal Matrix Metalloproteinase-3 and-9 Disrupts Spatial Memory
Wright, J. W., Brown, T. E., & Harding, J. W. (2013)

Authors: Nagy, V., Bozdagi, O., & Huntley, G. W.
Affiliations: Icahn School of Medicine at Mount Sinai (US)
ORCID: Nagy, Vanja
Huntley, George W.
Venue: Learning & Memory
Publisher: Cold Spring Harbor Laboratory
Published: 2007-09-25
Volume: 14
Issue: 10
Pages: 655-664
ISSN: 1072-0502 (ISSN-L)
1549-5485
DOI: 10.1101/lm.678307
PMC: PMC2044557
OpenAlex: W2119591418
Cited by: 107
References: 91
Citations by year: 2026: 2 · 2025: 2 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 4 · 2020: 6 · 2019: 10 · 2018: 3 · 2017: 9 · 2016: 3 · 2015: 9 · 2014: 5 · 2013: 8 · 2012: 10
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Learning & Memory (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Public Health Service
National Institute of Mental Health (R01MH075783, MH075783-01)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Keywords: MMP-9, passive avoidance learning, long-term memory consolidation, hippocampus, synaptic plasticity, matrix metalloproteinase inhibition, gelatinase inhibitors, extracellular proteolysis, memory impairment
MeSH terms: Animals, Avoidance Learning, Electroshock, Enzyme Induction, Hippocampus, Male, Nerve Tissue Proteins, Reaction Time, Retention, Psychology, Time Factors, Rats, Sprague-Dawley, Long-Term Potentiation, Rats, Long-Evans, Matrix Metalloproteinase 9, Rats, Matrix Metalloproteinase Inhibitors

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The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory

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