Cited by 208Protease and Inhibitor MechanismsNeuroscience and Neuropharmacology ResearchNeuroinflammation and Neurodegeneration Mechanisms

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MMPs in learning and memory and neuropsychiatric disorders

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Beroun, Anna, Mitra, Shiladitya, Michaluk, Piotr, Pijet, Barbara, Stefaniuk, Marzena, Kaczmarek, Leszek·2019·Cellular and Molecular Life Sciences

DOI 10.1007/s00018-019-03180-8PMC PMC6647627

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Abstract

Matrix metalloproteinases (MMPs) are a group of over twenty proteases, operating chiefly extracellularly to cleave components of the extracellular matrix, cell adhesion molecules as well as cytokines and growth factors. By virtue of their expression and activity patterns in animal models and clinical investigations, as well as functional studies with gene knockouts and enzyme inhibitors, MMPs have been demonstrated to play a paramount role in many physiological and pathological processes in the brain. In particular, they have been shown to influence learning and memory processes, as well as major neuropsychiatric disorders such as schizophrenia, various kinds of addiction, epilepsy, fragile X syndrome, and depression. A possible link connecting all those conditions is either physiological or aberrant synaptic plasticity where some MMPs, e.g., MMP-9, have been demonstrated to contribute to the structural and functional reorganization of excitatory synapses that are located on dendritic spines. Another common theme linking the aforementioned pathological conditions is neuroinflammation and MMPs have also been shown to be important mediators of immune responses.

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ELEVATION OF MATRIX METALLOPROTEINASES 3 AND 9 IN CEREBROSPINAL FLUID AND BLOOD IN PATIENTS WITH SEVERE TRAUMATIC BRAIN INJURY
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Microtubule-Dependent Matrix Metalloproteinase-2/Matrix Metalloproteinase-9 Exocytosis
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Role for MMP-9 in stress-induced downregulation of nectin-3 in hippocampal CA1 and associated behavioural alterations
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Differential vesicular distribution and trafficking of MMP‐2, MMP‐9, and their inhibitors in astrocytes
Sbai, O., Ould‐Yahoui, A., Ferhat, L., Gueye, Y., Bernard, A., Charrat, E., Mehanna, A., Risso, J., Chauvin, J., Fenouillet, E., et al. (2009) · Glia · doi:10.1002/glia.20927 · Cited by 138
Tissue inhibitor of metalloproteinases-1 (TIMP-1) is differentially induced in neurons and astrocytes after seizures: evidence for developmental, immediate early gene, and lesion response.
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Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases
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Metallothionein reduces central nervous system inflammation, neurodegeneration, and cell death following kainic acid‐induced epileptic seizures
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Activity-Dependent Local Translation of Matrix Metalloproteinase-9
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Minocycline treatment reverses ultrasonic vocalization production deficit in a mouse model of Fragile X Syndrome
Rotschafer, S. E., Trujillo, M. S., Dansie, L. E., Ethell, I. M., & Razak, K. A. (2012) · Brain Research · doi:10.1016/j.brainres.2011.12.041 · Cited by 130
Extracellular Matrix Plasticity and GABAergic Inhibition of Prefrontal Cortex Pyramidal Cells Facilitates Relapse to Heroin Seeking
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Matrix metalloproteinase‐2 (MMP‐2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins
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Tissue Inhibitor of Metalloproteinases-2 (TIMP-2) Suppresses TKR-Growth Factor Signaling Independent of Metalloproteinase Inhibition
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Role of matrix metalloproteinases in the acquisition and reconsolidation of cocaine-induced conditioned place preference
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Gene Expression in Human Hippocampus from Cocaine Abusers Identifies Genes which Regulate Extracellular Matrix Remodeling
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Ghrelin attenuates kainic acid-induced neuronal cell death in the mouse hippocampus.
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Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome
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Influence of Therapeutic Hypothermia on Matrix Metalloproteinase Activity after Traumatic Brain Injury in Rats
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Matrix metalloproteinase‐3 in the central nervous system: a look on the bright side
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The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses.
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Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration
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Matrix Metalloproteinase 9 in Epilepsy: The Role of Neuroinflammation in Seizure Development
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Electrocortical changes associated with minocycline treatment in fragile X syndrome
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Membrane-type 5 matrix metalloproteinase is expressed in differentiated neurons and regulates axonal growth.
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Membrane Localization of Membrane Type 5 Matrix Metalloproteinase by AMPA Receptor Binding Protein and Cleavage of Cadherins
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Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction
Michaluk, P., & Kaczmarek, L. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402141 · Cited by 103
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Stromelysin-1 (MMP-3) in synovial fluid of patients with rheumatoid arthritis has potential to cleave membrane bound Fas ligand.
Matsuno, H., Yudoh, K., Watanabe, Y., Nakazawa, F., Aono, H., & Kimura, T. (2001) · PubMed · Cited by 101
High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses
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Plasma levels of mature brain-derived neurotrophic factor (BDNF) and matrix metalloproteinase-9 (MMP-9) in treatment-resistant schizophrenia treated with clozapine.
Yamamori, H., Hashimoto, R., Ishima, T., Kishi, F., Yasuda, Y., Ohi, K., Fujimoto, M., Umeda-Yano, S., Ito, A., Hashimoto, K., et al. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.09.059 · Cited by 101 · cited 1×
“Similarly, upregulated MMP-9 serum levels were found to be strongly associated with levels of mature BDNF (MMP-9 aids in the formation of mature BDNF from pro-BDNF) in schizophrenia patients [232].”
Background
Matrix metalloproteinase‐7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation
Bilousova, T. V., Rusakov, D. A., Ethell, D. W., & Ethell, I. M. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03701.x · Cited by 98
Matrix metalloproteinase (MMP) system in brain: identification and characterization of brain-specific MMP highly expressed in cerebellum.
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Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells
Sbai, O., Ferhat, L., Bernard, A., Gueye, Y., Ould‐Yahoui, A., Thiolloy, S., Charrat, E., Charton, G., Tremblay, E. C., Risso, J., et al. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.08.004 · Cited by 97
Effects of matrix metalloproteinase inhibition on short‐ and long‐term plasticity of schaffer collateral/CA1 synapses
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Brain matrix metalloproteinase 1 levels are elevated in Alzheimer's disease
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Increased serum matrix metalloproteinase-9 (MMP-9) levels in young patients during bipolar depression
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Reward Learning Requires Activity of Matrix Metalloproteinase-9 in the Central Amygdala
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Feasibility of investigating differential proteomic expression in depression: implications for biomarker development in mood disorders
Frye, M. A., Nassan, M. M., Jenkins, G. D., Kung, S., Veldić, M., Palmer, B. A., Feeder, S. E., Tye, S. J., Choi, D., & Biernacka, J. M. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.185 · Cited by 89
Abnormality in serum levels of mature brain-derived neurotrophic factor (BDNF) and its precursor proBDNF in mood-stabilized patients with bipolar disorder: A study of two independent cohorts
Södersten, K., Pålsson, E., Ishima, T., Funa, K., Landén, M., Hashimoto, K., & Ågren, H. (2014) · Journal of Affective Disorders · doi:10.1016/j.jad.2014.01.009 · Cited by 86
Disruption of the blood–brain barrier after generalized tonic-clonic seizures correlates with cerebrospinal fluid MMP-9 levels
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Ethanol-induced impairment of spatial memory and brain matrix metalloproteinases
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Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats
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Cytotoxicity by Matrix Metalloprotease-1 in Organotypic Spinal Cord and Dissociated Neuronal Cultures
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miR-132 Regulates Dendritic Spine Structure by Direct Targeting of Matrix Metalloproteinase 9 mRNA
Jasińska, M., Miłek, J., Cymerman, I. A., Łęski, S., Kaczmarek, L., & Dziembowska, M. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9383-z · Cited by 83
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Synaptically released matrix metalloproteinase activity in control of structural plasticity and the cell surface distribution of GluA1-AMPA receptors
Szepesi, Z., Hosy, E., Ruszczycki, B., Bijata, M., Pyskaty, M., Bikbaev, A., Heine, M., Choquet, D., Kaczmarek, L., & Wlodarczyk, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098274 · Cited by 83
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Matrix metalloproteinase‐3 expression profile differentiates adaptive and maladaptive synaptic plasticity induced by traumatic brain injury
Falo, M. C., Fillmore, H. L., Reeves, T. M., & Phillips, L. L. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20986 · Cited by 83
Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-Fos pathway
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Elevation of hippocampal MMP-3 expression and activity during trauma-induced synaptogenesis
Kim, H. J., Fillmore, H. L., Reeves, T. M., & Phillips, L. L. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.10.014 · Cited by 81
Serum Levels of Matrix Metalloproteinases: Implications in Clinical Neurology
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Peptide Inhibition of Catalytic and Noncatalytic Activities of Matrix Metalloproteinase-9 Blocks Tumor Cell Migration and Invasion
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Matrix Metalloproteinases and Their Inhibitors in the Developing Mouse Brain and Spinal Cord: A Reverse Transcription Quantitative Polymerase Chain Reaction Study
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Differential spatio-temporal regulation of MMPs in the 5xFAD mouse model of Alzheimerâ€™s disease: evidence for a pro-amyloidogenic role of MT1-MMP
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Neural ECM proteases in learning and synaptic plasticity
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Functional polymorphism of the matrix metalloproteinase-9 (MMP-9) gene in schizophrenia.
Rybakowski, J. K., Skibinska, M., Kapelski, P., Kaczmarek, L., & Hauser, J. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.02.005 · Cited by 76
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Autism phenotypes in ZnT3 null mice: Involvement of zinc dyshomeostasis, MMP-9 activation and BDNF upregulation
Yoo, M. H., Kim, T.-Y., Yoon, Y. H., & Koh, J. (2016) · Scientific Reports · doi:10.1038/srep28548 · Cited by 76
Reduction of methamphetamine‐induced sensitization and reward in matrix metalloproteinase‐2 and ‐9‐deficient mice
Mizoguchi, H., Yamada, K., Niwa, M., Mouri, A., Mizuno, T., Noda, Y., Nitta, A., Itohara, S., Banno, Y., & Nabeshima, T. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04288.x · Cited by 75
Comparison of matrix metalloproteinase expression during Wallerian degeneration in the central and peripheral nervous systems
Hughes, P., Wells, G., Perry, V. H., Brown, M. C., & Miller, K. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00183-5 · Cited by 75
Transient ECM protease activity promotes synaptic plasticity
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Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures
Suenaga, N., Ichiyama, T., Kubota, M., Isumi, H., Tohyama, J., & Furukawa, S. (2007) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.09.011 · Cited by 73
Amniotic Fluid MMP ‐9 and Neurotrophins in Autism Spectrum Disorders: An Exploratory Study
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Matrix metalloproteinase-9 (MMP-9) in human intractable epilepsy caused by focal cortical dysplasia
Konopka, A., Grajkowska, W., Ziemiańska, K., Roszkowski, M., Daszkiewicz, P., Rysz, A., Marchel, A., Koperski, Ł., Wilczynski, G. M., & Dzwonek, J. (2012) · Epilepsy Research · doi:10.1016/j.eplepsyres.2012.09.018 · Cited by 72
Matrix Metalloproteinases Regulate the Formation of Dendritic Spine Head Protrusions during Chemically Induced Long-Term Potentiation
Szepesi, Z., Bijata, M., Ruszczycki, B., Kaczmarek, L., & Włodarczyk, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063314 · Cited by 72
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Elevation of MMP-9 Levels Promotes Epileptogenesis After Traumatic Brain Injury
Pijet, B., Stefaniuk, M., Kostrzewska-Księżyk, A., Tsilibary, P.-E., Tzinia, A. K., & Kaczmarek, L. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1061-5 · Cited by 71
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The tetrapartite synapse: Extracellular matrix remodeling contributes to corticoaccumbens plasticity underlying drug addiction
Smith, A. C. W., Scofield, M. D., & Kalivas, P. W. (2015) · Brain Research · doi:10.1016/j.brainres.2015.03.027 · Cited by 71
Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine‐induced behavioral sensitization and reward: implications for dopamine receptor down‐regulation and dopamine release
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Inhibition of hippocampal matrix metalloproteinase-3 and -9 disrupts spatial memory
Wright, J. W., Brown, T. E., & Harding, J. W. (2007) · Neural Plasticity · doi:10.1155/2007/73813 · Cited by 71
Gene expression profiling in treatment-naive schizophrenia patients identifies abnormalities in biological pathways involving AKT1 that are corrected by antipsychotic medication
Kumarasinghe, N., Beveridge, N. J., Gardiner, E. J., Scott, R. J., Yasawardene, S. G., Perera, A., Mendis, J., Suriyakumara, K., Schall, U., & Tooney, P. A. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000035 · Cited by 70
Matrix Metalloproteinase-9 and Synaptic Plasticity in the Central Amygdala in Control of Alcohol-Seeking Behavior
Stefaniuk, M., Beroun, A., Lebitko, T., Markina, O. A., Łęski, S., Meyza, K. Z., Grzywacz, A., Samochowiec, J., Samochowiec, A., Radwańska, K., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.12.026 · Cited by 70
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Adult ADHD vs. Bipolar Disorder in the DSM-5 Era: A Challenging Differentiation for Clinicians
BRUS, M. J., SOLANTO, M. V., & GOLDBERG, J. F. (2014) · Journal of Psychiatric Practice · doi:10.1097/01.pra.0000456591.20622.9e · Cited by 70
Expression of anti-cardiolipin antibodies and inflammatory associated factors in patients with schizophrenia
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MT5-MMP, ADAM-10, and N-Cadherin Act in Concert To Facilitate Synapse Reorganization after Traumatic Brain Injury
Harrell, K. M., Reeves, T. M., & Phillips, L. L. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2383 · Cited by 69
Caregiver burden in bipolar hypomania and mania: a systematic review.
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Dynamic Changes of Proteases and Protease Inhibitors Revealed by Microarray Analysis in CA3 and Entorhinal Cortex during Epileptogenesis in the Rat
Gorter, J. A., van Vliet, E. A., Rauwerda, H., Breit, T. M., Stad, R. K., Schaik, L. V., Vreugdenhil, E., Redeker, S., Hendriksen, E., Aronica, E., et al. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2007.01290.x · Cited by 69
Latent MMP-9 is bound to TIMP-1 before secretion
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Blocking human fear memory with the matrix metalloproteinase inhibitor doxycycline
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The role of MMP-9 in integrin-mediated hippocampal cell death after pilocarpine-induced status epilepticus
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Matrix Metalloproteinase-7 Regulates Cleavage of Pro-Nerve Growth Factor and Is Neuroprotective following Kainic Acid-Induced Seizures
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Matrix metalloproteinase-9 activity increased by two different types of epileptic seizures that do not induce neuronal death: A possible role in homeostatic synaptic plasticity
Takács, E., Nyilas, R., Szepesi, Z., Baracskay, P., Karlsen, B., Røsvold, T., Bjørkum, A. A., Czurkó, A., Kovács, Z., Kékesi, A. K., et al. (2010) · Neurochemistry International · doi:10.1016/j.neuint.2010.03.003 · Cited by 63
Abnormal intrinsic dynamics of dendritic spines in a fragile X syndrome mouse model in vivo
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MATRIX METALLOPROTEINASE-9 AND TISSUE INHIBITORS OF METALLOPROTEINASES 1 IN INFLUENZA-ASSOCIATED ENCEPHALOPATHY
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Authors: Beroun, A., Mitra, S., Michaluk, P., Pijet, B., Stefaniuk, M., & Kaczmarek, L.
Affiliations: Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
Corresponding author: Kaczmarek, Leszek
ORCID: Beroun, Anna
Mitra, Shiladitya
Michaluk, Piotr
Pijet, Barbara
Stefaniuk, Marzena
Kaczmarek, Leszek
Venue: Cellular and Molecular Life Sciences
Publisher: Springer Science and Business Media LLC
Published: 2019-06-06
Volume: 76
Issue: 16
Pages: 3207-3228
ISSN: 1420-682X (ISSN-L)
1420-9071
DOI: 10.1007/s00018-019-03180-8
PMC: PMC6647627
OpenAlex: W2954884521
Cited by: 207
References: 269
Citations by year: 2026: 16 · 2025: 24 · 2024: 34 · 2023: 31 · 2022: 40 · 2021: 25 · 2020: 32 · 2019: 4
FWCI: 2.44
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Cellular and Molecular Life Sciences (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Foundation for Polish Science (BRAINCITY)
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 › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: matrix metalloproteinases, MMP-9, learning and memory, neuropsychiatric disorders, schizophrenia, addiction, epilepsy, fragile X syndrome, depression, synaptic plasticity, dendritic spines, neuroinflammation, extracellular matrix, cytokines and growth factors
MeSH terms: Animals, Mental Disorders, Brain, Epilepsy, Humans, Learning, Memory, Neuronal Plasticity, Tissue Inhibitor of Metalloproteinases, Matrix Metalloproteinases

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