The DOI matches its Crossref record; 269 of the 269 references it cites were found in a registry or an index.
MMPs in learning and memory and neuropsychiatric disorders
Open accessAbstract
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“The ECM can be modified rapidly by the release of proteases [36], by microglial action and by internalization, all of which can be activated by memory events [37–39].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [37]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Items 201–269 of 269
Matrix metalloproteinase-9 may be a potential therapeutic target in epilepsy
Yin, P., Yang, L., Zhou, H. Y., & Sun, R. P. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.09.013 · Cited by 42
The Search for an Effective Therapy to Treat Fragile X Syndrome: Dream or Reality?
Castagnola, S., Bardoni, B., & Maurin, T. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00015 · Cited by 42
Cell Type- and Tissue Context-dependent Nuclear Distribution of Human Ago2
Sharma, N. R., Wang, X., Majerčiak, V., Ajiro, M., Kruhlak, M. J., Meyers, C., & Zheng, Z. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.c115.695049 · Cited by 41
Aujla, P. K., & Huntley, G. W. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23468 · Cited by 39
Expression and Activity of Metalloproteinases in Depression
Bobińska, K., Szemraj, J., Czarny, P. L., & Gałecki, P. (2016) · Medical Science Monitor · doi:10.12659/msm.895978 · Cited by 39
von Gertten, C., Holmin, S., Mathiesen, T. I., & Nordqvist, A. S. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10729 · Cited by 39
Involvement of matrix metalloproteinase-9 in the development of morphine tolerance
Nakamoto, K., Kawasaki, S., Kobori, T., Fujita‐Hamabe, W., Mizoguchi, H., Yamada, K., Nabeshima, T., & Tokuyama, S. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.03.006 · Cited by 39
Lepeta, K., Purzycka, K. J., Pachulska‐Wieczorek, K., Mitjans, M., Begemann, M., Vafadari, B., Bijata, K., Adamiak, R. W., Ehrenreich, H., Dziembowska, M., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201707723 · Cited by 39
Self-citationBajor, M., Michaluk, P., Gulyássy, P., Kékesi, K. A., Juhász, G. D., & Kaczmarek, L. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07829.x · Cited by 38
Self-citationMurphy, N., & Lynch, M. A. (2012) · Journal of Neurochemistry · doi:10.1111/jnc.12031 · Cited by 37
Wójtowicz, T., & Mozrzymas, J. W. (2013) · Hippocampus · doi:10.1002/hipo.22205 · Cited by 37
The role of MMP genes in recurrent depressive disorders and cognitive functions
Bobińska, K., Szemraj, J., Gałecki, P., & Talarowska, M. E. (2016) · Acta Neuropsychiatrica · doi:10.1017/neu.2015.72 · Cited by 36
Roles of Matrix Metalloproteinases and Their Targets in Epileptogenesis and Seizures
Mizoguchi, H., & Yamada, K. (2013) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2013.11.2.45 · Cited by 35
Towards a modern classification of the epilepsies?
Berg, A. T., & Cross, J. H. (2010) · The Lancet Neurology · doi:10.1016/s1474-4422(10)70024-7 · Cited by 35
Hippocampal MMP-3 elevation is associated with passive avoidance conditioning
Olson, M. L., Meighan, P. C., Brown, T. E., Asay, A. L., Benoist, C. C., Harding, J. W., & Wright, J. W. (2007) · Regulatory Peptides · doi:10.1016/j.regpep.2007.07.004 · Cited by 35
Ontogeny of MMPs and TIMPs in the murine neocortex.
Bednarek, N., Clément, Y., Lelièvre, V., Olivier, P., Loron, G., Garnotel, R., & Gressens, P. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e3181973aee · Cited by 35
Roberts, D. J., Jenne, C. N., Léger, C., Kramer, A. H., Gallagher, C., Todd, S., Parney, I. F., Doig, C. J., Yong, V. W., Kubes, P., et al. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2012.2841 · Cited by 35
An Aberrant Cerebellar Development in Mice Lacking Matrix Metalloproteinase-3
Hove, I. V., Verslegers, M., Buyens, T., Delorme, N., Lemmens, K., Stroobants, S., Gantois, I., D’Hooge, R., & Moons, L. (2011) · Molecular Neurobiology · doi:10.1007/s12035-011-8215-z · Cited by 34
Lee, H., Lee, E., Song, Y. S., & Kim, E. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0158 · Cited by 34
Brzdąk, P., Wójcicka, O., Zaręba-Kozioł, M., Minge, D., Henneberger, C., Włodarczyk, J., Mozrzymas, J. W., & Wójtowicz, T. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx324 · Cited by 34
Altered neuronal architecture and plasticity in the visual cortex of adult MMP-3-deficient mice
Aerts, J., Nys, J., Moons, L., Hu, T., & Arckens, L. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0819-4 · Cited by 34
Epigenetics of Epileptogenesis-Evoked Upregulation of Matrix Metalloproteinase-9 in Hippocampus
Żybura-Broda, K., Amborska, R., Ambrożek-Latecka, M., Wilemska, J., Bogusz, A., Bucko, J., Konopka, A., Grajkowska, W., Roszkowski, M., Marchel, A., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159745 · Cited by 34
Self-citationQuírico‐Santos, T., Mello, A. L. D. N., Gomes, A. C., Carvalho, L. F. P. P. D. C., de Souza, J. M., & Alves‐Leon, S. V. (2013) · Brain Research · doi:10.1016/j.brainres.2013.09.044 · Cited by 33
Gupta, R. K., Awasthi, R., Garg, R. K., Kumar, N., Gupta, P. K., Singh, A. K., Sahoo, P., Paliwal, V. K., Prasad, K. N., Pandey, C. M., et al. (2012) · American Journal of Neuroradiology · doi:10.3174/ajnr.a3346 · Cited by 33
Wang, Q., Ishikawa, T., Michiue, T., Zhu, B.-L., Guan, D., & Maeda, H. (2014) · International Journal of Legal Medicine · doi:10.1007/s00414-014-0972-6 · Cited by 32
Valente, M. M., Allen, M., Bortolotto, V., Seung Taik, L. I. M., Conant, K. E., & Grilli, M. (2015) · Neural Plasticity · doi:10.1155/2015/646595 · Cited by 32
MMP‐7 (matrilysin) expression in human brain tumors
Rome, C., Arsaut, J., Taris, C., Couillaud, F., & Loiseau, H. (2007) · Molecular Carcinogenesis · doi:10.1002/mc.20293 · Cited by 32
Traumatische Erinnerungen medikamentös abschwächen
(2017) · Fortschritte der Neurologie · Psychiatrie · doi:10.1055/s-0043-111154 · Cited by 31
Natarajan, R., Harding, J. W., & Wright, J. W. (2013) · Journal of Experimental Neuroscience · doi:10.4137/jen.s11381 · Cited by 30
WRIGHT, J., Meighan, S. E., MURPHY, E., Holtfreter, K. L., Davis, C. J., OLSON, M., Benoist, C. C., Muhunthan, K., & Harding, J. W. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.006 · Cited by 30
Relationship between methamphetamine exposure and matrix metalloproteinase 9 expression
Liu, Y., Brown, S., Shaikh, J., Fishback, J. A., & Matsumoto, R. R. (2008) · Neuroreport · doi:10.1097/wnr.0b013e32830dd606 · Cited by 29
Szklarczyk, A., Oyler, G. A., McKay, R. D. G., Gerfen, C. R., & Conant, K. E. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04625.x · Cited by 29
Groef, L. D., Andries, L., Lemmens, K., Hove, I. V., & Moons, L. (2015) · BMC Ophthalmology · doi:10.1186/s12886-015-0176-y · Cited by 29
Górkiewicz, T., Szczuraszek, K., Wyrembek, P., Michaluk, P., Kaczmarek, L., & Mozrzymas, J. W. (2009) · Hippocampus · doi:10.1002/hipo.20736 · Cited by 29
Self-citationMatrix metalloproteinases and epileptogenesis
Ikonomidou, C. (2014) · Molecular and Cellular Pediatrics · doi:10.1186/s40348-014-0006-y · Cited by 28
Increased Expression of Matrix Metalloproteinase-9 in Patients with Temporal Lobe Epilepsy
Acar, G., Tanrιöver, G., Acar, F., & Demir, R. (2014) · Turkish Neurosurgery · doi:10.5137/1019-5149.jtn.10738-14.0 · Cited by 28
Hoehna, Y., Uckermann, O., Luksch, H., Stefovska, V. G., Marzahn, J., Theil, M., Górkiewicz, T., Gawlak, M., Wilczynski, G. M., Kaczmarek, L., et al. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.06.023 · Cited by 27
Self-citationKelly, E. A., Tremblay, M., Gahmberg, C. G., Tian, L., & Majewska, A. K. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23440 · Cited by 27
Localization of proteinase expression in the developing rabbit brain
Bigio, M. R. D., & Jacque, C. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(95)00023-7 · Cited by 25
Gossas, T., & Danielson, U. H. (2006) · Biochemical Journal · doi:10.1042/bj20051933 · Cited by 25
Rahimi, S., Sayad, A., Moslemi, E., Ghafouri-Fard, S., & Taheri, M. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0043-z · Cited by 24
McGregor, N. W., Thompson, N., O’Connell, K. S., Emsley, R. A., van der Merwe, L., & Warnich, L. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.01.044 · Cited by 24
Lundberg, A. K., Jönsson, S., Stenmark, J., Kristenson, M., & Jonasson, L. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.07.219 · Cited by 24
Regulation of expression of stromyelysin-1 by proinflammatory cytokines in mouse brain astrocytes.
Witek-Zawada, B., & Koj, A. (2003) · PubMed · Cited by 23
Networks of blood proteins in the neuroimmunology of schizophrenia
Jeffries, C. D., Perkins, D. O., Fournier, M., Kim, Q., Cuénod, M., Khadimallah, I., Domenici, E., Addington, J., Bearden, C. E., Cadenhead, K. S., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0158-y · Cited by 23
Han, H., He, X., Tang, J., Liu, W., Liu, K., Zhang, J., Wang, X., Xu, Y., & Chen, X. (2011) · Psychiatry Research · doi:10.1016/j.psychres.2011.04.026 · Cited by 22
Niedringhaus, M. S., Chen, X., Conant, K. E., & Dzakpasu, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057144 · Cited by 22
Alterations in serum MMP and TIMP concentrations following chronic heroin abuse
Kovatsi, L., Batzios, S., Nikolaou, K., Fragou, D., Njau, S., Tsatsakis, A., Karakiulakis, G., & Papakonstantinou, E. (2013) · Toxicology Mechanisms and Methods · doi:10.3109/15376516.2012.758681 · Cited by 21
Pielecka-Fortuna, J., Kalogeraki, E., Fortuna, M. G., & Löwel, S. (2015) · eLife · doi:10.7554/elife.11290 · Cited by 21
DP-b99 Modulates Matrix Metalloproteinase Activity and Neuronal Plasticity
Yeghiazaryan, M., Rutkowska-Włodarczyk, I., Konopka, A., Wilczynski, G. M., Melikyan, A., Korkotian, E., Kaczmarek, L., & Figiel, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099789 · Cited by 19
Self-citationHabituation-induced neural plasticity in the hippocampus and prefrontal cortex mediated by MMP-3
Wright, J. W., Meighan, P. C., Brown, T. E., Wiediger, R. V., Sorg, B. A., & Harding, J. W. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.014 · Cited by 18
Serum matrix metalloproteinase-2: A potential biomarker for diagnosis of epilepsy
Wang, R., Zeng, G. Q., Tong, R. Z., Zhou, D., & Hong, Z. (2016) · Epilepsy Research · doi:10.1016/j.eplepsyres.2016.02.009 · Cited by 18
Aguayo, F. I., Pacheco, A., García‐Rojo, G., Pizarro-Bäuerle, J., Doberti, A. V., Tejos‐Bravo, M., García-Pérez, M. A., Rojas, P. S., & Fiedler, J. L. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00387 · Cited by 18
Shahar, E. M., Attias, U., Savulescu, D. M., Genizin, J., Gavish, M., & Nagler, R. M. (2013) · Epilepsy Research · doi:10.1016/j.eplepsyres.2013.10.003 · Cited by 17
Matrix metalloproteinase-9 gene modulates prefrontal cognition in bipolar men
RYBAKOWSKI, J. K., Skibińska, M., Leszczyńska-Rodziewicz, A., Kaczmarek, L., & Hauser, J. (2009) · Psychiatric Genetics · doi:10.1097/ypg.0b013e32832080be · Cited by 15
Self-citationCazzin, C., Mion, S., Caldara, F., Rimland, J. M., & Domenici, E. (2010) · Molecular Biology Reports · doi:10.1007/s11033-010-0193-0 · Cited by 15
Matsumoto, J., Hirano, Y., Hashimoto, K., Ishima, T., Kanahara, N., Niitsu, T., Shiina, A., Hashimoto, T., Sato, Y., Yokote, K., et al. (2016) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12490 · Cited by 15
Küçükali, C. İ., Aydın, M., Özkök, E., Bilge, E., Orhan, N., Türkmen, A. Z., & Kara, İ. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.02.012 · Cited by 14
Gregory, M. D., Kippenhan, J. S., Callicott, J. H., Rubinstein, D., Mattay, V. S., Coppola, R., & Berman, K. F. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy344 · Cited by 13
Epilepsy: structural or functional?
Stevens, J. (1996) · PubMed Central · Cited by 12
Wiediger, R. V., & Wright, J. W. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.009 · Cited by 11
Ierusalimsky, V. N., & Balaban, P. M. (2013) · Acta Histochemica · doi:10.1016/j.acthis.2013.04.001 · Cited by 9
Drago, A., Monti, B., Ronchi, D. D., & Serretti, A. (2014) · Neuropsychobiology · doi:10.1159/000356971 · Cited by 8
Verzeaux, L., Belloy, N., Thevenard-Devy, J., Devy, J., Ferracci, G., Martiny, L., Dedieu, S., Dauchez, M., Emonard, H., Etique, N., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-05039-z · Cited by 8
Novel odors affect gene expression for cytokines and proteinases in the rat amygdala and hippocampus
Irwin, L. N., & Byers, D. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.10.034 · Cited by 6
Nassan, M. M., Jia, Y., Jenkins, G. D., Colby, C. L., Feeder, S. E., Choi, D., Veldić, M., McElroy, S. L., Bond, D. J., Weinshilboum, R. M., et al. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.07.005 · Cited by 5
Kordower (1999) · doi:10.1002/1531-8249(199909)46:3
Collins (1998) · doi:10.1002/(sici)1097-4652(199807)176:1
(1998) · Europe PMC (PubMed Central)
Cited by
Sorted by citations
de Almeida, L. G. N., Thode, H., Eslambolchi, Y., Chopra, S., Young, D. W., Gill, S. E., Devel, L., & Dufour, A. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000349 · Cited by 572
Behl, T., Kaur, G., Sehgal, A., Bhardwaj, S., Singh, S., Buhaș, C. L., Pusta, C. T. J., Uivaroșan, D., Munteanu, M. A., & BUNGAU, S. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031413 · Cited by 198
The extracellular matrix and perineuronal nets in memory
Fawcett, J. W., Fyhn, M., Jendelova, P., Kwok, J. C. F., Ruzicka, J., & Sorg, B. A. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01634-3 · Cited by 169
Venturino, A., Schulz, R., De Jesús-Cortés, H., Maes, M. E., Nagy, B., Reilly-Andújar, F., Colombo, G., Cubero, R. J. A., Schoot Uiterkamp, F. E., Bear, M. F., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109313 · Cited by 140
Seney, M. L., Kim, S.-M., Glausier, J. R., Hildebrand, M. A., Xue, X., Zong, W., Wang, J., Shelton, M. A., Phan, B. N., Srinivasan, C., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.06.007 · Cited by 135
Metadata
- 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
- Venue
- Cellular and Molecular Life Sciences
- Published
- 2019-06-06
- Volume
- 76
- Issue
- 16
- Pages
- 3207-3228
- ISSN
- 1420-682X (ISSN-L)
- 1420-9071
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
