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Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately

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Wang, Xiao-bin, Bozdagi, Ozlem, Nikitczuk, Jessica S., Zhai, Zu Wei, Zhou, Qiang, Huntley, George W.·2008·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0807248105PMC PMC2614793

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Abstract

Persistent dendritic spine enlargement is associated with stable long-term potentiation (LTP), and the latter is thought to underlie long-lasting memories. Extracellular proteolytic remodeling of the synaptic microenvironment could be important for such plasticity, but whether or how proteolytic remodeling contributes to persistent modifications in synapse structure and function is unknown. Matrix metalloproteinase-9 (MMP-9) is an extracellular protease that is activated perisynaptically after LTP induction and required for LTP maintenance. Here, by monitoring spine size and excitatory postsynaptic potentials (EPSPs) simultaneously with combined 2-photon time-lapse imaging and whole-cell recordings from hippocampal neurons, we find that MMP-9 is both necessary and sufficient to drive spine enlargement and synaptic potentiation concomitantly. Both structural and functional MMP-driven forms of plasticity are mediated through β1-containing integrin receptors, are associated with integrin-dependent cofilin inactivation within spines, and require actin polymerization. In contrast, postsynaptic exocytosis and protein synthesis are both required for MMP-9-induced potentiation, but not for initial MMP-9-induced spine expansion. However, spine expansion becomes unstable when postsynaptic exocytosis or protein synthesis is blocked, indicating that the 2 forms of plasticity are expressed independently but require interactions between them for persistence. When MMP activity is eliminated during theta-stimulation-induced LTP, both spine enlargement and synaptic potentiation are transient. Thus, MMP-mediated extracellular remodeling during LTP has an instructive role in establishing persistent modifications in both synapse structure and function of the kind critical for learning and memory.

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Authors: Wang, X.-B., Bozdagi, O., Nikitczuk, J. S., Zhai, Z. W., Zhou, Q., & Huntley, G. W.
Affiliations: Departments of aNeurology and
Icahn School of Medicine at Mount Sinai (US)
ORCID: Zhai, Zu Wei
Zhou, Qiang
Huntley, George W.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2008-12-09
Volume: 105
Issue: 49
Pages: 19520-19525
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0807248105
PMC: PMC2614793
OpenAlex: W1977637789
Cited by: 316
References: 48
Citations by year: 2026: 5 · 2025: 9 · 2024: 10 · 2023: 10 · 2022: 14 · 2021: 13 · 2020: 22 · 2019: 17 · 2018: 23 · 2017: 15 · 2016: 20 · 2015: 21 · 2014: 26 · 2013: 23 · 2012: 32
FWCI: 8.07
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Ellison Medical Foundation
Whitehall Foundation
National Institute of Mental Health (R01MH075783, MH-075783)
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 › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: MMP-9, long-term potentiation, synaptic plasticity, extracellular proteolysis, beta1 integrin, cofilin, actin polymerization, protein synthesis, hippocampal neurons, memory formation
MeSH terms: Actins, Animals, Exocytosis, Extracellular Matrix, Neuronal Plasticity, Phosphorylation, Integrins, Rats, Sprague-Dawley, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Matrix Metalloproteinase 9, Dendritic Spines, Actin Depolymerizing Factors, Rats

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Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately

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