Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses
Open accessAbstract
Long-term synaptic plasticity is shaped by the controlled reorganization of the synaptic proteome. A key component of this process is local proteolysis performed by the family of extracellular matrix metalloproteinases (MMPs). In recent years, considerable progress was achieved in identifying extracellular proteases involved in neuroplasticity phenomena and their protein substrates. Perisynaptic metalloproteinases regulate plastic changes at synapses through the processing of extracellular and membrane proteins. MMP9 was found to play a crucial role in excitatory synapses by controlling the NMDA-dependent LTP component. In addition, MMP3 regulates the L-type calcium channel-dependent form of LTP as well as the plasticity of neuronal excitability. Both MMP9 and MMP3 were implicated in memory and learning. Moreover, altered expression or mutations of different MMPs are associated with learning deficits and psychiatric disorders, including schizophrenia, addiction, or stress response. Contrary to excitatory drive, the investigation into the role of extracellular proteolysis in inhibitory synapses is only just beginning. Herein, we review the principal mechanisms of MMP involvement in the plasticity of excitatory transmission and the recently discovered role of proteolysis in inhibitory synapses. We discuss how different matrix metalloproteinases shape dynamics and turnover of synaptic adhesome and signal transduction pathways in neurons. Finally, we discuss future challenges in exploring synapse- and plasticity-specific functions of different metalloproteinases.
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
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?
Modification of the CNS ECM by activity-related release of metalloproteinases can cause rapid changes in PNNs in region of synapses, enabling local changes in synaptic properties.
“An important mechanism of plasticity is modification of the CNS ECM by activity-related release of metalloproteinases, which can cause rapid changes in PNNs in region of synapses, enabling local changes in synaptic properties [38, 58].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [58]
The Introduction (section 1; page unavailable) says neuronal activity can prompt MMP secretion and activation, locally loosening ECM and changing synaptic structure and efficacy. Sections 2.2 and 3.1 link MMPs or PNNs to plasticity, but do not establish that activity-related MMP release causes rapid PNN changes specifically near synapses. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Control of Synaptic Strength by Glial TNFα
Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattie, M. S., & Malenka, R. C. (2002) · Science · doi:10.1126/science.1067859 · Cited by 1,344 · see citing works
Memory engrams: Recalling the past and imagining the future
Josselyn, S. A., & Tonegawa, S. (2020) · Science · doi:10.1126/science.aaw4325 · Cited by 1,087 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
Fawcett, J. W., Oohashi, T., & Pizzorusso, T. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0196-3 · Cited by 589 · see citing works
Backstrom, J. R., Lim, G. P., Cullen, M. J., & Tökés, Z. A. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-24-07910.1996 · Cited by 331 · cited 1× · see citing works
“Finally, neuronal MMP9 may cleave and degrade β-amyloid peptide in brains of patients suffering from the Alzheimer’s disease [92].”
BackgroundWang, X.-B., Bozdagi, O., Nikitczuk, J. S., Zhai, Z. W., Zhou, Q., & Huntley, G. W. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807248105 · Cited by 316 · see citing works
Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology
Michaluk, P., Wawrzyniak, M., Alot, P., Szczot, M., Wyrembek, P., Mercik, K., Medvedev, N., Wilczek, E., De Roo, M., Zuschratter, W., et al. (2011) · Journal of Cell Science · doi:10.1242/jcs.090852 · Cited by 214 · see citing works
Self-citationGkogkas, C. G., Khoutorsky, A., Cao, R., Jafarnejad, S. M., Prager-Khoutorsky, M., Giannakas, N., Kaminari, A., Fragkouli, A., Nader, K., Price, T. J., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.064 · Cited by 201 · see citing works
Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons
Mardinly, A. R., Spiegel, I., Patrizi, A., Centofante, E., Bazinet, J. E., Tzeng, C. P., Mandel-Brehm, C., Harmin, D. A., Adesnik, H., Fagiolini, M., et al. (2016) · Nature · doi:10.1038/nature17187 · Cited by 176 · see citing works
Shaping Synapses by the Neural Extracellular Matrix
Ferrer-Ferrer, M., & Dityatev, A. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00040 · Cited by 169 · see citing works
Wen, T. H., Afroz, S., Reinhard, S. M., Palacios, A. R., Tapia, K., Binder, D. K., Razak, K. A., & Ethell, I. M. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhx258 · Cited by 165 · see citing works
Muir, J., Arancibia-Carcamo, I. L., MacAskill, A. F., Smith, K. R., Griffin, L. D., & Kittler, J. T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000589107 · Cited by 158 · see citing works
Inhibitory engrams in perception and memory
Barron, H. C., Vogels, T. P., Behrens, T. E., & Ramaswami, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701812114 · Cited by 147 · see citing works
Hausrat, T. J., Muhia, M., Gerrow, K., Thomas, P., Hirdes, W., Tsukita, S., Heisler, F. F., Herich, L., Dubroqua, S., Breiden, P., et al. (2015) · Nature Communications · doi:10.1038/ncomms7872 · Cited by 138 · see citing works
Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses
Foscarin, S., Ponchione, D., Pajaj, E., Leto, K., Gawlak, M., Wilczynski, G. M., Rossi, F., & Carulli, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016666 · Cited by 128 · see citing works
Brown, T. E., Forquer, M. R., Cocking, D. L., Jansen, H. T., Harding, J. W., & Sorg, B. A. (2007) · Learning & Memory · doi:10.1101/lm.476207 · Cited by 121 · see citing works
Carceller, H., Guirado, R., Ripolles-Campos, E., Teruel-Marti, V., & Nacher, J. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0291-20.2020 · Cited by 112 · see citing works
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 · see citing works
Murase, S., Lantz, C. L., & Quinlan, E. M. (2017) · eLife · doi:10.7554/elife.27345 · Cited by 87 · see citing works
Alaiyed, S., McCann, M., Mahajan, G., Rajkowska, G., Stockmeier, C. A., Kellar, K. J., Wu, J. Y., & Conant, K. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.2387-19.2020 · Cited by 84 · see citing works
Metalloproteinase inhibition prevents inhibitory synapse reorganization and seizure genesis
Pollock, E., Everest, M., Brown, A., & Poulter, M. O. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.06.003 · Cited by 75 · see citing works
Releasing Addiction Memories Trapped in Perineuronal Nets
Lasek, A. W., Chen, H., & Chen, W.-Y. (2018) · Trends in Genetics · doi:10.1016/j.tig.2017.12.004 · Cited by 71 · see citing works
Increased metalloproteinase activity in the hippocampus following status epilepticus
Dubey, D., McRae, P. A., Rankin-Gee, E. K., Baranov, E., Wandrey, L., Rogers, S., & Porter, B. E. (2017) · Epilepsy Research · doi:10.1016/j.eplepsyres.2017.02.021 · Cited by 65 · see citing works
Spolidoro, M., Putignano, E., Munafò, C., Maffei, L., & Pizzorusso, T. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr158 · Cited by 58 · see citing works
Wiera, G., Wozniak, G., Bajor, M., Kaczmarek, L., & Mozrzymas, J. W. (2013) · Hippocampus · doi:10.1002/hipo.22112 · Cited by 57 · see citing works
Kelly, E. A., Russo, A. S., Jackson, C. D., Lamantia, C. E., & Majewska, A. K. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00369 · Cited by 48 · see citing works
Flagged first, then by citations
Research works printed but not linked: 165
- [1]Choi J.H. Sim S.E. Interregional synaptic maps among engram cells underlie memory formation Science 2018 360 430 435 10.1126/science.aas9204 29700265 · DOI
- [3]Abdou K. Shehata M. Choko K. Nishizono H. Matsuo M. Muramatsu S.I. Inokuchi K. Synapse-specific representation of the identity of overlapping memory engrams Science 2018 360 1227 1231 10.1126/science.aat3810 29903972 · DOI
- [4]Dityatev A. Rusakov D.A. Molecular signals of plasticity at the tetrapartite synapse Curr. Opin. Neurobiol. 2011 21 353 359 10.1016/j.conb.2010.12.006 21277196 PMC3368316 · DOI · Paper page
- [5]Smith A.C. Scofield M.D. Kalivas P.W. The tetrapartite synapse: Extracellular matrix remodeling contributes to corticoaccumbens plasticity underlying drug addiction Brain Res. 2015 1628 29 39 10.1016/j.brainres.2015.03.027 25838241 PMC4589426 · DOI · Paper page
- [8]Sonderegger P. Matsumoto-Miyai K. Activity-controlled proteolytic cleavage at the synapse Trends Neurosci. 2014 37 413 423 10.1016/j.tins.2014.05.007 24969462 · DOI
- [9]Vafadari B. Salamian A. Kaczmarek L. Mmp-9 in translation: From molecule to brain physiology, pathology, and therapy J. Neurochem. 2016 139 Suppl. S2 91 114 10.1111/jnc.13415 26525923 · DOI
- [10]Brzdak P. Nowak D. Wiera G. Mozrzymas J.W. Multifaceted roles of metzincins in cns physiology and pathology: From synaptic plasticity and cognition to neurodegenerative disorders Front. Cell. Neurosci. 2017 11 178 10.3389/fncel.2017.00178 28713245 PMC5491558 · DOI
- [11]Huntley G.W. Synaptic circuit remodelling by matrix metalloproteinases in health and disease Nat. Rev. Neurosci. 2012 13 743 757 10.1038/nrn3320 23047773 PMC4900464 · DOI
- [12]Piccard H. Van den Steen P.E. Opdenakker G. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins J. Leukoc. Biol. 2007 81 870 892 10.1189/jlb.1006629 17185359 · DOI
- [13]Brew K. Nagase H. The tissue inhibitors of metalloproteinases (timps): An ancient family with structural and functional diversity Biochim. Biophys. Acta 2010 1803 55 71 10.1016/j.bbamcr.2010.01.003 20080133 PMC2853873 · DOI
- [14]Etique N. Verzeaux L. Dedieu S. Emonard H. Lrp-1: A checkpoint for the extracellular matrix proteolysis Biomed. Res. Int. 2013 2013 152163 10.1155/2013/152163 23936774 PMC3723059 · DOI
- [15]Gomis-Rüth F.X. Structural aspects of the metzincin clan of metalloendopeptidases Mol. Biotechnol. 2003 24 157 202 10.1385/MB:24:2:157 12746556 · DOI
- [16]Vandooren J. Van den Steen P.E. Opdenakker G. Biochemistry and molecular biology of gelatinase b or matrix metalloproteinase-9 (mmp-9): The next decade Crit Rev. Biochem. Mol. Biol. 2013 48 222 272 10.3109/10409238.2013.770819 23547785 · DOI
- [17]Tsien R.Y. Very long-term memories may be stored in the pattern of holes in the perineuronal net Proc. Natl. Acad. Sci. USA 2013 110 12456 12461 10.1073/pnas.1310158110 23832785 PMC3725115 · DOI · Paper page
- [18]Wiera G. Nowak D. van Hove I. Dziegiel P. Moons L. Mozrzymas J.W. Mechanisms of nmda receptor- and voltage-gated l-type calcium channel-dependent hippocampal ltp critically rely on proteolysis that is mediated by distinct metalloproteinases J. Neurosci. Off. J. Soc. Neurosci. 2017 37 1240 1256 10.1523/JNEUROSCI.2170-16.2016 PMC6596865 28069922 · DOI
- [19]Wiera G. Lebida K. Lech A.M. Brzdąk P. Van Hove I. De Groef L. Moons L. Petrini E.M. Barberis A. Mozrzymas J.W. Long-term plasticity of inhibitory synapses in the hippocampus and spatial learning depends on matrix metalloproteinase 3 Cell. Mol. Life Sci. CMLS 2021 78 2279 2298 10.1007/s00018-020-03640-6 32959071 PMC7966195 · DOI
- [20]Zhang J.W. Deb S. Gottschall P.E. Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration Eur. J. Neurosci. 1998 10 3358 3368 10.1046/j.1460-9568.1998.00347.x 9824449 · DOI
- [21]Fazeli M.S. Errington M.L. Dolphin A.C. Bliss T.V. Increased efflux of a haemoglobin-like protein and an 80 kda protease into push-pull perfusates following the induction of long-term potentiation in the dentate gyrus Brain Res. 1990 521 247 253 10.1016/0006-8993(90)91549-V 2207664 · DOI
- [22]Vandooren J. Geurts N. Martens E. Van den Steen P.E. Opdenakker G. Zymography methods for visualizing hydrolytic enzymes Nat. Methods 2013 10 211 220 10.1038/nmeth.2371 23443633 · DOI
- [23]Fazeli M.S. Breen K. Errington M.L. Bliss T.V. Increase in extracellular ncam and amyloid precursor protein following induction of long-term potentiation in the dentate gyrus of anaesthetized rats Neurosci. Lett. 1994 169 77 80 10.1016/0304-3940(94)90360-3 8047297 · DOI
- [24]Qian Z. Gilbert M.E. Colicos M.A. Kandel E.R. Kuhl D. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation Nature 1993 361 453 457 10.1038/361453a0 8429885 · DOI
- [25]Nedivi E. Hevroni D. Naot D. Israeli D. Citri Y. Numerous candidate plasticity-related genes revealed by differential cdna cloning Nature 1993 363 718 722 10.1038/363718a0 8515813 · DOI
- [26]Chiao Y.A. Ramirez T.A. Zamilpa R. Okoronkwo S.M. Dai Q. Zhang J. Jin Y.F. Lindsey M.L. Matrix metalloproteinase-9 deletion attenuates myocardial fibrosis and diastolic dysfunction in ageing mice Cardiovasc. Res. 2012 96 444 455 10.1093/cvr/cvs275 22918978 PMC3500048 · DOI
- [27]Li C.K. Pender S.L. Pickard K.M. Chance V. Holloway J.A. Huett A. Goncalves N.S. Mudgett J.S. Dougan G. Frankel G. Impaired immunity to intestinal bacterial infection in stromelysin-1 (matrix metalloproteinase-3)-deficient mice J. Immunol. 2004 173 5171 5179 10.4049/jimmunol.173.8.5171 15470062 · DOI
- [28]Vanden Berghe T. Hulpiau P. Martens L. Vandenbroucke R.E. Van Wonterghem E. Perry S.W. Bruggeman I. Divert T. Choi S.M. Vuylsteke M. Passenger mutations confound interpretation of all genetically modified congenic mice Immunity 2015 43 200 209 10.1016/j.immuni.2015.06.011 26163370 PMC4800811 · DOI
- [29]De Bruyn M. Breynaert C. Arijs I. De Hertogh G. Geboes K. Thijs G. Matteoli G. Hu J. Van Damme J. Arnold B. Inhibition of gelatinase b/mmp-9 does not attenuate colitis in murine models of inflammatory bowel disease Nat. Commun. 2017 8 15384 10.1038/ncomms15384 28561062 PMC5460016 · DOI
- [30]Lisman J. Criteria for identifying the molecular basis of the engram (camkii, pkmzeta) Mol. Brain 2017 10 55 10.1186/s13041-017-0337-4 29187215 PMC5707903 · DOI
- [32]Nagy V. Bozdagi O. Matynia A. Balcerzyk M. Okulski P. Dzwonek J. Costa R.M. Silva A.J. Kaczmarek L. Huntley G.W. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory J. Neurosci. Off. J. Soc. Neurosci. 2006 26 1923 1934 10.1523/JNEUROSCI.4359-05.2006 16481424 PMC4428329 · DOI · Paper page
- [34]Wiera G. Mozrzymas J.W. Extracellular proteolysis in structural and functional plasticity of mossy fiber synapses in hippocampus Front. Cell. Neurosci. 2015 9 427 10.3389/fncel.2015.00427 26582976 PMC4631828 · DOI
- [35]Gorkiewicz T. Balcerzyk M. Kaczmarek L. Knapska E. Matrix metalloproteinase 9 (mmp-9) is indispensable for long term potentiation in the central and basal but not in the lateral nucleus of the amygdala Front. Cell. Neurosci. 2015 9 73 10.3389/fncel.2015.00073 25814930 PMC4356064 · DOI
- [37]Bozdagi O. Nagy V. Kwei K.T. Huntley G.W. In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity J. Neurophysiol. 2007 98 334 344 10.1152/jn.00202.2007 17493927 PMC4415272 · DOI · Paper page
- [38]Wojtowicz T. Mozrzymas J.W. Late phase of long-term potentiation in the mossy fiber-ca3 hippocampal pathway is critically dependent on metalloproteinases activity Hippocampus 2010 20 917 921 10.1002/hipo.20787 20572195 · DOI
- [39]Meighan S.E. Meighan P.C. Choudhury P. Davis C.J. Olson M.L. Zornes P.A. Wright J.W. Harding J.W. Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity J. Neurochem. 2006 96 1227 1241 10.1111/j.1471-4159.2005.03565.x 16464240 · DOI
- [40]Dziembowska M. Milek J. Janusz A. Rejmak E. Romanowska E. Gorkiewicz T. Tiron A. Bramham C.R. Kaczmarek L. Activity-dependent local translation of matrix metalloproteinase-9 J. Neurosci. Off. J. Soc. Neurosci. 2012 32 14538 14547 10.1523/JNEUROSCI.6028-11.2012 23077039 PMC6621441 · DOI
- [41]Janusz A. Milek J. Perycz M. Pacini L. Bagni C. Kaczmarek L. Dziembowska M. The fragile x mental retardation protein regulates matrix metalloproteinase 9 mrna at synapses J. Neurosci. Off. J. Soc. Neurosci. 2013 33 18234 18241 10.1523/JNEUROSCI.2207-13.2013 PMC6619756 24227732 · DOI · Paper page
- [42]Jasinska M. Milek J. Cymerman I.A. Leski S. Kaczmarek L. Dziembowska M. Mir-132 regulates dendritic spine structure by direct targeting of matrix metalloproteinase 9 mrna Mol. Neurobiol. 2016 53 4701 4712 10.1007/s12035-015-9383-z 26319558 PMC4965491 · DOI
- [43]Sbai O. Ferhat L. Bernard A. Gueye Y. Ould-Yahoui A. Thiolloy S. Charrat E. Charton G. Tremblay E. Risso J.J. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells Mol. Cell. Neurosci. 2008 39 549 568 10.1016/j.mcn.2008.08.004 18817873 · DOI
- [44]Harward S.C. Hedrick N.G. Hall C.E. Parra-Bueno P. Milner T.A. Pan E. Laviv T. Hempstead B.L. Yasuda R. McNamara J.O. Autocrine bdnf-trkb signalling within a single dendritic spine Nature 2016 538 99 103 10.1038/nature19766 27680698 PMC5398094 · DOI · Paper page
- [45]Lu H. Park H. Poo M.M. Spike-timing-dependent bdnf secretion and synaptic plasticity Philos. Trans. R. Soc. Lond. Ser. Bbiological. Sci. 2014 369 20130132 10.1098/rstb.2013.0132 24298135 PMC3843865 · DOI
- [46]Park M. Salgado J.M. Ostroff L. Helton T.D. Robinson C.G. Harris K.M. Ehlers M.D. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes Neuron 2006 52 817 830 10.1016/j.neuron.2006.09.040 17145503 PMC1899130 · DOI · Paper page
- [47]Murphy G. Nagase H. Localizing matrix metalloproteinase activities in the pericellular environment Febs J. 2011 278 2 15 10.1111/j.1742-4658.2010.07918.x 21087456 PMC3004722 · DOI
- [48]Dzwonek J. Wilczynski G.M. Cd44: Molecular interactions, signaling and functions in the nervous system Front. Cell. Neurosci. 2015 9 175 10.3389/fncel.2015.00175 25999819 PMC4423434 · DOI
- [49]Stawarski M. Stefaniuk M. Wlodarczyk J. Matrix metalloproteinase-9 involvement in the structural plasticity of dendritic spines Front. Neuroanat. 2014 8 68 10.3389/fnana.2014.00068 25071472 PMC4091410 · DOI
- [50]Szepesi Z. Hosy E. Ruszczycki B. Bijata M. Pyskaty M. Bikbaev A. Heine M. Choquet D. Kaczmarek L. Wlodarczyk J. Synaptically released matrix metalloproteinase activity in control of structural plasticity and the cell surface distribution of glua1-ampa receptors PLoS ONE 2014 9 e98274 10.1371/journal.pone.0098274 24853857 PMC4031140 · DOI · Paper page
- [51]Ogata Y. Enghild J.J. Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9 J. Biol. Chem. 1992 267 3581 3584 10.1016/S0021-9258(19)50563-4 1371271 · DOI
- [52]Manabe S. Gu Z. Lipton S.A. Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to nmda-induced retinal ganglion cell death Invest. Ophthalmol. Vis. Sci. 2005 46 4747 4753 10.1167/iovs.05-0128 16303975 · DOI
- [53]O’Sullivan S. Medina C. Ledwidge M. Radomski M.W. Gilmer J.F. Nitric oxide-matrix metaloproteinase-9 interactions: Biological and pharmacological significance--no and mmp-9 interactions Biochim. Biophys. Acta 2014 1843 603 617 10.1016/j.bbamcr.2013.12.006 24333402 · DOI
- [54]Gu Z. Kaul M. Yan B. Kridel S.J. Cui J. Strongin A. Smith J.W. Liddington R.C. Lipton S.A. S-nitrosylation of matrix metalloproteinases: Signaling pathway to neuronal cell death Science 2002 297 1186 1190 10.1126/science.1073634 12183632 · DOI · Paper page
- [55]Peppin G.J. Weiss S.J. Activation of the endogenous metalloproteinase, gelatinase, by triggered human neutrophils Proc. Natl. Acad. Sci. USA 1986 83 4322 4326 10.1073/pnas.83.12.4322 3012563 PMC323724 · DOI
- [56]Padamsey Z. McGuinness L. Bardo S.J. Reinhart M. Tong R. Hedegaard A. Hart M.L. Emptage N.J. Activity-dependent exocytosis of lysosomes regulates the structural plasticity of dendritic spines Neuron 2017 93 132 146 10.1016/j.neuron.2016.11.013 27989455 PMC5222721 · DOI · Paper page
- [57]Bijata M. Labus J. Guseva D. Stawarski M. Butzlaff M. Dzwonek J. Schneeberg J. Bohm K. Michaluk P. Rusakov D.A. Synaptic remodeling depends on signaling between serotonin receptors and the extracellular matrix Cell Rep. 2017 19 1767 1782 10.1016/j.celrep.2017.05.023 28564597 · DOI
- [58]Figiel I. Kruk P.K. Zareba-Koziol M. Rybak P. Bijata M. Wlodarczyk J. Dzwonek J. Mmp-9 signaling pathways that engage rho gtpases in brain plasticity Cells 2021 10 166 10.3390/cells10010166 33467671 PMC7830260 · DOI
- [59]Bajor M. Kaczmarek L. Proteolytic remodeling of the synaptic cell adhesion molecules (cams) by metzincins in synaptic plasticity Neurochem. Res. 2013 38 1113 1121 10.1007/s11064-012-0919-6 23124395 PMC3653053 · DOI
- [60]Shinoe T. Goda Y. Tuning synapses by proteolytic remodeling of the adhesive surface Curr. Opin. Neurobiol. 2015 35 148 155 10.1016/j.conb.2015.08.005 26318535 · DOI
- [62]Peixoto R.T. Kunz P.A. Kwon H. Mabb A.M. Sabatini B.L. Philpot B.D. Ehlers M.D. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1 Neuron 2012 76 396 409 10.1016/j.neuron.2012.07.006 23083741 PMC3783515 · DOI
- [63]Chmielewska J.J. Kuzniewska B. Milek J. Urbanska K. Dziembowska M. Neuroligin 1, 2, and 3 regulation at the synapse: Fmrp-dependent translation and activity-induced proteolytic cleavage Mol. Neurobiol. 2019 56 2741 2759 10.1007/s12035-018-1243-1 30056576 PMC6459971 · DOI
- [64]Ribot J. Breton R. Calvo C.-F. Moulard J. Ezan P. Zapata J. Samama K. Moreau M. Bemelmans A.-P. Sabatet V. Astrocytes close the mouse critical period for visual plasticity Science 2021 373 77 81 10.1126/science.abf5273 34210880 · DOI
- [65]Mizoguchi H. Nakade J. Tachibana M. Ibi D. Someya E. Koike H. Kamei H. Nabeshima T. Itohara S. Takuma K. Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-bdnf to mature bdnf in the hippocampus J. Neurosci. Off. J. Soc. Neurosci. 2011 31 12963 12971 10.1523/JNEUROSCI.3118-11.2011 21900575 PMC6623408 · DOI
- [66]Niculescu D. Michaelsen-Preusse K. Güner Ü. van Dorland R. Wierenga C.J. Lohmann C. A bdnf-mediated push-pull plasticity mechanism for synaptic clustering Cell Rep. 2018 24 2063 2074 10.1016/j.celrep.2018.07.073 30134168 · DOI
- [67]Cao W. Duan J. Wang X. Zhong X. Hu Z. Huang F. Wang H. Zhang J. Li F. Zhang J. Early enriched environment induces an increased conversion of probdnf to bdnf in the adult rat’s hippocampus Behav. Brain Res. 2014 265 76 83 10.1016/j.bbr.2014.02.022 24569010 · DOI · Paper page
- [68]Kuzniewska B. Rejmak E. Malik A.R. Jaworski J. Kaczmarek L. Kalita K. Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-fos pathway Mol. Cell Biol. 2013 33 2149 2162 10.1128/MCB.00008-13 23508111 PMC3648073 · DOI · Paper page
- [71]Murase S. Winkowski D. Liu J. Kanold P.O. Quinlan E.M. Homeostatic regulation of perisynaptic matrix metalloproteinase 9 (mmp9) activity in the amblyopic visual cortex eLife 2019 8 e52503 10.7554/eLife.52503 31868167 PMC6961978 · DOI
- [73]Garcia-Keller C. Neuhofer D. Bobadilla A.C. Spencer S. Chioma V.C. Monforton C. Kalivas P.W. Extracellular matrix signaling through beta3 integrin mediates cocaine cue-induced transient synaptic plasticity and relapse Biol. Psychiatry 2019 86 377 387 10.1016/j.biopsych.2019.03.982 31126696 PMC6697624 · DOI
- [74]Michaluk P. Mikasova L. Groc L. Frischknecht R. Choquet D. Kaczmarek L. Matrix metalloproteinase-9 controls nmda receptor surface diffusion through integrin beta1 signaling J. Neurosci. Off. J. Soc. Neurosci. 2009 29 6007 6012 10.1523/JNEUROSCI.5346-08.2009 19420267 PMC6665240 · DOI
- [76]Ricard-Blum S. Vallet S.D. Proteases decode the extracellular matrix cryptome Biochimie 2016 122 300 313 10.1016/j.biochi.2015.09.016 26382969 · DOI
- [77]Ning L. Tian L. Smirnov S. Vihinen H. Llano O. Vick K. Davis R.L. Rivera C. Gahmberg C.G. Interactions between icam-5 and beta1 integrins regulate neuronal synapse formation J. Cell Sci. 2013 126 77 89 23015592 PMC3603512
- [78]Kelly E.A. Tremblay M.E. Gahmberg C.G. Tian L. Majewska A.K. Interactions between intercellular adhesion molecule-5 positive elements and their surroundings in the rodent visual cortex Commun. Integr. Biol. 2013 6 e27315 10.4161/cib.27315 24753788 PMC3984291 · DOI
- [79]Kelly E.A. Tremblay M.E. Gahmberg C.G. Tian L. Majewska A.K. Subcellular localization of intercellular adhesion molecule-5 (telencephalin) in the visual cortex is not developmentally regulated in the absence of matrix metalloproteinase-9 J. Comp. Neurol. 2014 522 676 688 10.1002/cne.23440 23897576 PMC3877171 · DOI
- [80]Lonskaya I. Partridge J. Lalchandani R.R. Chung A. Lee T. Vicini S. Hoe H.S. Lim S.T. Conant K. Soluble icam-5, a product of activity dependent proteolysis, increases mepsc frequency and dendritic expression of glua1 PLoS ONE 2013 8 e69136 10.1371/journal.pone.0069136 23844251 PMC3699500 · DOI
- [81]Kramar E.A. Lin B. Rex C.S. Gall C.M. Lynch G. Integrin-driven actin polymerization consolidates long-term potentiation Proc. Natl. Acad. Sci. USA 2006 103 5579 5584 10.1073/pnas.0601354103 16567651 PMC1459396 · DOI · Paper page
- [82]Babayan A.H. Kramar E.A. Barrett R.M. Jafari M. Haettig J. Chen L.Y. Rex C.S. Lauterborn J.C. Wood M.A. Gall C.M. Integrin dynamics produce a delayed stage of long-term potentiation and memory consolidation J. Neurosci. Off. J. Soc. Neurosci. 2012 32 12854 12861 10.1523/JNEUROSCI.2024-12.2012 PMC3752079 22973009 · DOI · Paper page
- [83]Meighan P.C. Meighan S.E. Davis C.J. Wright J.W. Harding J.W. Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of schaffer collateral/ca1 synapses J. Neurochem. 2007 102 2085 2096 10.1111/j.1471-4159.2007.04682.x 17587312 · DOI
- [84]Lebida K. Mozrzymas J.W. Spike timing-dependent plasticity in the mouse barrel cortex is strongly modulated by sensory learning and depends on activity of matrix metalloproteinase 9 Mol. Neurobiol. 2017 54 6723 6736 10.1007/s12035-016-0174-y 27744572 PMC5622912 · DOI
- [85]Magnowska M. Gorkiewicz T. Suska A. Wawrzyniak M. Rutkowska-Wlodarczyk I. Kaczmarek L. Wlodarczyk J. Transient ecm protease activity promotes synaptic plasticity Sci. Rep. 2016 6 27757 10.1038/srep27757 27282248 PMC4901294 · DOI
- [86]Cauwe B. Van den Steen P.E. Opdenakker G. The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases Crit. Rev. Biochem. Mol. Biol. 2007 42 113 185 10.1080/10409230701340019 17562450 · DOI
- [87]Cauwe B. Opdenakker G. Intracellular substrate cleavage: A novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases Crit. Rev. Biochem. Mol. Biol. 2010 45 351 423 10.3109/10409238.2010.501783 20812779 · DOI
- [88]Prudova A. auf dem Keller U. Butler G.S. Overall C.M. Multiplex n-terminome analysis of mmp-2 and mmp-9 substrate degradomes by itraq-tails quantitative proteomics Mol. Cell Proteom. 2010 9 894 911 10.1074/mcp.M000050-MCP201 PMC2871422 20305284 · DOI
- [90]Heir R. Stellwagen D. Tnf-mediated homeostatic synaptic plasticity: From in vitro to in vivo models Front. Cell. Neurosci. 2020 14 565841 10.3389/fncel.2020.565841 33192311 PMC7556297 · DOI
- [91]Valenzuela J.C. Heise C. Franken G. Singh J. Schweitzer B. Seidenbecher C.I. Frischknecht R. Hyaluronan-based extracellular matrix under conditions of homeostatic plasticity Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2014 369 20130606 10.1098/rstb.2013.0606 25225099 PMC4173291 · DOI
- [93]Abramov E. Dolev I. Fogel H. Ciccotosto G.D. Ruff E. Slutsky I. Amyloid-beta as a positive endogenous regulator of release probability at hippocampal synapses Nat. Neurosci. 2009 12 1567 1576 10.1038/nn.2433 19935655 · DOI · Paper page
- [94]Castellano J.M. Mosher K.I. Abbey R.J. McBride A.A. James M.L. Berdnik D. Shen J.C. Zou B. Xie X.S. Tingle M. Human umbilical cord plasma proteins revitalize hippocampal function in aged mice Nature 2017 544 488 492 10.1038/nature22067 28424512 PMC5586222 · DOI · Paper page
- [95]Baba Y. Yasuda O. Takemura Y. Ishikawa Y. Ohishi M. Iwanami J. Mogi M. Doe N. Horiuchi M. Maeda N. Timp-3 deficiency impairs cognitive function in mice Lab. Investig. A J. Tech. Methods Pathol. 2009 89 1340 1347 10.1038/labinvest.2009.101 PMC3047444 19806081 · DOI
- [96]Jaworski D.M. Boone J. Caterina J. Soloway P. Falls W.A. Prepulse inhibition and fear-potentiated startle are altered in tissue inhibitor of metalloproteinase-2 (timp-2) knockout mice Brain Res. 2005 1051 81 89 10.1016/j.brainres.2005.05.057 15979591 · DOI
- [97]Okulski P. Jay T.M. Jaworski J. Duniec K. Dzwonek J. Konopacki F.A. Wilczynski G.M. Sanchez-Capelo A. Mallet J. Kaczmarek L. Timp-1 abolishes mmp-9-dependent long-lasting long-term potentiation in the prefrontal cortex Biol. Psychiatry 2007 62 359 362 10.1016/j.biopsych.2006.09.012 17210139 · DOI
- [98]Wiera G. Wojtowicz T. Lebida K. Piotrowska A. Drulis-Fajdasz D. Gomulkiewicz A. Gendosz D. Podhorska-Okolow M. Capogna M. Wilczynski G. Long term potentiation affects intracellular metalloproteinases activity in the mossy fiber-ca3 pathway Mol. Cell. Neurosci. 2012 50 147 159 10.1016/j.mcn.2012.04.005 22555058 · DOI
- [99]Ganguly K. Rejmak E. Mikosz M. Nikolaev E. Knapska E. Kaczmarek L. Matrix metalloproteinase (mmp) 9 transcription in mouse brain induced by fear learning J. Biol. Chem. 2013 288 20978 20991 10.1074/jbc.M113.457903 23720741 PMC3774367 · DOI
- [100]Van der Kooij M.A. Fantin M. Rejmak E. Grosse J. Zanoletti O. Fournier C. Ganguly K. Kalita K. Kaczmarek L. Sandi C. Role for mmp-9 in stress-induced downregulation of nectin-3 in hippocampal ca1 and associated behavioural alterations Nat. Commun. 2014 5 4995 10.1038/ncomms5995 25232752 PMC4199199 · DOI · Paper page
- [102]Knapska E. Lioudyno V. Kiryk A. Mikosz M. Gorkiewicz T. Michaluk P. Gawlak M. Chaturvedi M. Mochol G. Balcerzyk M. Reward learning requires activity of matrix metalloproteinase-9 in the central amygdala J. Neurosci. Off. J. Soc. Neurosci. 2013 33 14591 14600 10.1523/JNEUROSCI.5239-12.2013 PMC6618374 24005309 · DOI
- [103]Chioma V.C. Kruyer A. Bobadilla A.C. Angelis A. Ellison Z. Hodebourg R. Scofield M.D. Kalivas P.W. Heroin seeking and extinction from seeking activate matrix metalloproteinases at synapses on distinct subpopulations of accumbens cells Biol. Psychiatry 2021 89 947 958 10.1016/j.biopsych.2020.12.004 33579535 PMC8434769 · DOI
- [104]Vandooren J. Born B. Solomonov I. Zajac E. Saldova R. Senske M. Ugarte-Berzal E. Martens E. Van den Steen P.E. Van Damme J. Circular trimers of gelatinase b/matrix metalloproteinase-9 constitute a distinct population of functional enzyme molecules differentially regulated by tissue inhibitor of metalloproteinases-1 Biochem. J. 2015 465 259 270 10.1042/BJ20140418 25360794 PMC4399976 · DOI
- [105]Serifova X. Ugarte-Berzal E. Homotrimeric mmp-9 is an active hitchhiker on alpha-2-macroglobulin partially escaping protease inhibition and internalization through lrp-1 Cell. Mol. Life Sci. 2020 77 3013 3026 10.1007/s00018-019-03338-4 31642940 PMC11104829 · DOI
- [106]Mizoguchi H. Ibi D. Takuma K. Toth E. Sato J. Itohara S. Nabeshima T. Yamada K. Alterations of emotional and cognitive behaviors in matrix metallo- proteinase-2 and -9-deficient mice Open Behav. Sci. J. 2010 4 19 25 10.2174/1874230001004010019 · DOI
- [107]Kaliszewska A. Bijata M. Kaczmarek L. Kossut M. Experience-dependent plasticity of the barrel cortex in mice observed with 2-dg brain mapping and c-fos: Effects of mmp-9 ko Cereb. Cortex 2012 22 2160 2170 10.1093/cercor/bhr303 22021911 · DOI · Paper page
- [109]Mizoguchi H. Yamada K. Mouri A. Niwa M. Mizuno T. Noda Y. Nitta A. Itohara S. Banno Y. Nabeshima T. 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 J. Neurochem. 2007 102 1548 1560 10.1111/j.1471-4159.2007.04623.x 17472698 · DOI
- [111]Smith A.C. Kupchik Y.M. Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases Nat. Neurosci. 2014 17 1655 1657 10.1038/nn.3846 25326689 PMC4241163 · DOI
- [112]Stefaniuk M. Beroun A. Lebitko T. Markina O. Leski S. Meyza K. Grzywacz A. Samochowiec J. Samochowiec A. Radwanska K. Matrix metalloproteinase-9 and synaptic plasticity in the central amygdala in control of alcohol-seeking behavior Biol. Psychiatry 2017 81 907 917 10.1016/j.biopsych.2016.12.026 28190519 · DOI
- [114]Salamian A. Legutko D. Nowicka K. Badyra B. Kazmierska-Grebowska P. Caban B. Kowalczyk T. Kaczmarek L. Beroun A. Inhibition of matrix metalloproteinase 9 activity promotes synaptogenesis in the hippocampus Cereb. Cortex 2021 31 3804 3819 10.1093/cercor/bhab050 33739386 PMC8258443 · DOI
- [115]Conant K. Wang Y. Szklarczyk A. Dudak A. Mattson M.P. Lim S.T. Matrix metalloproteinase-dependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation Neuroscience 2010 166 508 521 10.1016/j.neuroscience.2009.12.061 20045450 PMC3535483 · DOI
- [116]Brzdak P. Wlodarczyk J. Mozrzymas J.W. Wojtowicz T. Matrix metalloprotease 3 activity supports hippocampal epsp-to-spike plasticity following patterned neuronal activity via the regulation of nmdar function and calcium flux Mol. Neurobiol. 2017 54 804 816 10.1007/s12035-016-9970-7 27351676 PMC5219885 · DOI
- [117]Wójtowicz T. Mozrzymas J.W. Matrix metalloprotease activity shapes the magnitude of EPSPs and spike plasticity within the hippocampal CA3 network Hippocampus 2014 24 135 153 10.1002/hipo.22205 24115249 · DOI
- [118]Brzdak P. Wojcicka O. Zareba-Koziol M. Minge D. Henneberger C. Wlodarczyk J. Mozrzymas J.W. Wojtowicz T. Synaptic potentiation at basal and apical dendrites of hippocampal pyramidal neurons involves activation of a distinct set of extracellular and intracellular molecular cues Cereb. Cortex 2019 29 283 304 10.1093/cercor/bhx324 29228131 · DOI
- [119]Kochlamazashvili G. Henneberger C. Bukalo O. Dvoretskova E. Senkov O. Lievens P.M. Westenbroek R. Engel A.K. Catterall W.A. Rusakov D.A. The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic l-type Ca2+ channels Neuron 2010 67 116 128 10.1016/j.neuron.2010.05.030 20624596 PMC3378029 · DOI · Paper page
- [120]Morellini F. Malyshev A. Volgushev M. Chistiakova M. Papashvili G. Fellini L. Kleene R. Schachner M. Dityatev A. Impaired fear extinction due to a deficit in Ca2+ influx through l-type voltage-gated Ca2+ channels in mice deficient for tenascin-c Front. Integr. Neurosci. 2017 11 16 10.3389/fnint.2017.00016 28824389 PMC5539374 · DOI
- [121]Stegemann C. Didangelos A. Barallobre-Barreiro J. Langley S.R. Mandal K. Jahangiri M. Mayr M. Proteomic identification of matrix metalloproteinase substrates in the human vasculature Circ. Cardiovasc. Genet. 2013 6 106 117 10.1161/CIRCGENETICS.112.964452 23255316 · DOI
- [122]Falcon-Moya R. Perez-Rodriguez M. Prius-Mengual J. Andrade-Talavera Y. Arroyo-Garcia L.E. Perez-Artes R. Mateos-Aparicio P. Guerra-Gomes S. Oliveira J.F. Flores G. Astrocyte-mediated switch in spike timing-dependent plasticity during hippocampal development Nat. Commun. 2020 11 4388 10.1038/s41467-020-18024-4 32873805 PMC7463247 · DOI
- [123]Pigott B.M. Garthwaite J. Nitric oxide is required for l-type Ca2+ channel-dependent long-term potentiation in the hippocampus Front. Synaptic Neurosci. 2016 8 17 10.3389/fnsyn.2016.00017 27445786 PMC4925670 · DOI
- [124]Van Hove I. Lemmens K. Van de Velde S. Verslegers M. Moons L. Matrix metalloproteinase-3 in the central nervous system: A look on the bright side J. Neurochem. 2012 123 203 216 10.1111/j.1471-4159.2012.07900.x 22862420 · DOI
- [125]Matsuura T. Li X.H. Tao C. Zhuo M. Effects of matrix metalloproteinase inhibitors on n-methyl-d-aspartate receptor and contribute to long-term potentiation in the anterior cingulate cortex of adult mice Mol. Pain 2019 15 1744806919842958 10.1177/1744806919842958 30900509 PMC6480992 · DOI
- [126]Aerts J. Nys J. Moons L. Hu T.T. Arckens L. Altered neuronal architecture and plasticity in the visual cortex of adult mmp-3-deficient mice Brain Struct. Funct. 2015 220 2675 2689 10.1007/s00429-014-0819-4 24957860 · DOI
- [127]Van Hove I. Verslegers M. Buyens T. Delorme N. Lemmens K. Stroobants S. Gantois I. D’Hooge R. Moons L. An aberrant cerebellar development in mice lacking matrix metalloproteinase-3 Mol. Neurobiol. 2012 45 17 29 10.1007/s12035-011-8215-z 22108898 · DOI
- [128]Nowak D. Groef L. Moons L. Mozrzymas J.W. Mmp-3 deficiency does not influence the length and number of ca1 dendrites of hippocampus of adult mice Acta Neurobiol. Exp. 2018 78 281 286 10.21307/ane-2018-026 30295685 · DOI
- [129]Olson M.L. Meighan P.C. Brown T.E. Asay A.L. Benoist C.C. Harding J.W. Wright J.W. Hippocampal mmp-3 elevation is associated with passive avoidance conditioning Regul. Pept. 2008 146 19 25 10.1016/j.regpep.2007.07.004 17698214 · DOI
- [130]Wright J.W. Meighan P.C. Brown T.E. Wiediger R.V. Sorg B.A. Harding J.W. Habituation-induced neural plasticity in the hippocampus and prefrontal cortex mediated by mmp-3 Behav. Brain Res. 2009 203 27 34 10.1016/j.bbr.2009.04.014 19389428 · DOI
- [131]Pauly T. Ratliff M. Pietrowski E. Neugebauer R. Schlicksupp A. Kirsch J. Kuhse J. Activity-dependent shedding of the nmda receptor glycine binding site by matrix metalloproteinase 3: A putative mechanism of postsynaptic plasticity PLoS ONE 2008 3 e2681 10.1371/journal.pone.0002681 18629001 PMC2443283 · DOI
- [132]Franzke C.W. Tasanen K. Schacke H. Zhou Z. Tryggvason K. Mauch C. Zigrino P. Sunnarborg S. Lee D.C. Fahrenholz F. Transmembrane collagen xvii, an epithelial adhesion protein, is shed from the cell surface by adams Embo J. 2002 21 5026 5035 10.1093/emboj/cdf532 12356719 PMC129053 · DOI
- [133]Odake S. Morita Y. Morikawa T. Yoshida N. Hori H. Nagai Y. Inhibition of matrix metalloproteinases by peptidyl hydroxamic acids Biochem. Biophys. Res. Commun. 1994 199 1442 1446 10.1006/bbrc.1994.1392 8147888 · DOI
- [134]Lee H. Lee E.J. Song Y.S. Kim E. Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule ngl-3 through nmda receptors, matrix metalloproteinases and presenilin/gamma-secretase Philos. Trans. R Soc. Lond. B Biol. Sci. 2014 369 20130158 10.1098/rstb.2013.0158 24298159 PMC3843889 · DOI
- [135]Wilczynski G.M. Konopacki F.A. Wilczek E. Lasiecka Z. Gorlewicz A. Michaluk P. Wawrzyniak M. Malinowska M. Okulski P. Kolodziej L.R. Important role of matrix metalloproteinase 9 in epileptogenesis J. Cell Biol. 2008 180 1021 1035 10.1083/jcb.200708213 18332222 PMC2265409 · DOI · Paper page
- [136]Gorter J.A. Van Vliet E.A. Rauwerda H. Breit T. Stad R. van Schaik L. Vreugdenhil E. Redeker S. Hendriksen E. Aronica E. Dynamic changes of proteases and protease inhibitors revealed by microarray analysis in ca3 and entorhinal cortex during epileptogenesis in the rat Epilepsia 2007 48 Suppl. S5 53 64 10.1111/j.1528-1167.2007.01290.x 17910582 · DOI
- [138]Konopka A. Grajkowska W. Ziemianska K. Roszkowski M. Daszkiewicz P. Rysz A. Marchel A. Koperski L. Wilczynski G.M. Dzwonek J. Matrix metalloproteinase-9 (mmp-9) in human intractable epilepsy caused by focal cortical dysplasia Epilepsy Res. 2013 104 45 58 10.1016/j.eplepsyres.2012.09.018 23182966 · DOI
- [141]Szklarczyk A. Ewaleifoh O. Beique J.C. Wang Y. Knorr D. Haughey N. Malpica T. Mattson M.P. Huganir R. Conant K. Mmp-7 cleaves the nr1 nmda receptor subunit and modifies nmda receptor function Faseb J. 2008 22 3757 3767 10.1096/fj.07-101402 18644839 PMC2574025 · DOI
- [143]Szodorai E. Bampali K. Romanov R.A. Kasper S. Hokfelt T. Ernst M. Lubec G. Harkany T. Diversity matters: Combinatorial information coding by gabaa receptor subunits during spatial learning and its allosteric modulation Cell Signal. 2018 50 142 159 10.1016/j.cellsig.2018.07.003 30006122 · DOI
- [144]Barberis A. Postsynaptic plasticity of gabaergic synapses Neuropharmacology 2020 169 107643 10.1016/j.neuropharm.2019.05.020 31108109 · DOI
- [145]Chiu C.Q. Barberis A. Higley M.J. Preserving the balance: Diverse forms of long-term gabaergic synaptic plasticity Nat. Rev. Neurosci. 2019 20 272 281 10.1038/s41583-019-0141-5 30837689 · DOI
- [146]Capogna M. Castillo P.E. Maffei A. The ins and outs of inhibitory synaptic plasticity: Neuron types, molecular mechanisms and functional roles Eur. J. Neurosci. 2020 10.1111/ejn.14907 32663353 PMC9150441 · DOI
- [148]Castillo P.E. Chiu C.Q. Carroll R.C. Long-term plasticity at inhibitory synapses Curr. Opin. Neurobiol. 2011 21 328 338 10.1016/j.conb.2011.01.006 21334194 PMC3092861 · DOI · Paper page
- [149]Younts T.J. Castillo P.E. Endogenous cannabinoid signaling at inhibitory interneurons Curr. Opin. Neurobiol. 2014 26 42 50 10.1016/j.conb.2013.12.006 24650503 PMC4024354 · DOI
- [150]Chiu C.Q. Martenson J.S. Yamazaki M. Natsume R. Sakimura K. Tomita S. Tavalin S.J. Higley M.J. Input-specific nmdar-dependent potentiation of dendritic gabaergic inhibition Neuron 2018 97 368 377.e363 10.1016/j.neuron.2017.12.032 29346754 PMC5777295 · DOI
- [151]Petrini E.M. Ravasenga T. Hausrat T.J. Iurilli G. Olcese U. Racine V. Sibarita J.B. Jacob T.C. Moss S.J. Benfenati F. Synaptic recruitment of gephyrin regulates surface gabaa receptor dynamics for the expression of inhibitory ltp Nat. Commun. 2014 5 3921 10.1038/ncomms4921 24894704 PMC4059940 · DOI
- [153]Udakis M. Pedrosa V. Chamberlain S.E.L. Clopath C. Mellor J.R. Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto ca1 pyramidal neurons shapes hippocampal output Nat. Commun. 2020 11 4395 10.1038/s41467-020-18074-8 32879322 PMC7467931 · DOI
- [154]Kurotani T. Yamada K. Yoshimura Y. Crair M.C. Komatsu Y. State-dependent bidirectional modification of somatic inhibition in neocortical pyramidal cells Neuron 2008 57 905 916 10.1016/j.neuron.2008.01.030 18367091 PMC2880402 · DOI
- [155]Pigeat R. Chausson P. Dreyfus F.M. Leresche N. Lambert R.C. Sleep slow wave-related homo and heterosynaptic ltd of intrathalamic gabaaergic synapses: Involvement of t-type ca2+ channels and metabotropic glutamate receptors J. Neurosci. Off. J. Soc. Neurosci. 2015 35 64 73 10.1523/JNEUROSCI.2748-14.2015 25568103 PMC6605246 · DOI
- [156]Raimondo J.V. Richards B.A. Woodin M.A. Neuronal chloride and excitability—the big impact of small changes Curr. Opin. Neurobiol. 2017 43 35 42 10.1016/j.conb.2016.11.012 27992777 · DOI
- [157]Favuzzi E. Deogracias R. Marques-Smith A. Maeso P. Jezequel J. Exposito-Alonso D. Balia M. Kroon T. Hinojosa A.J. Maraver F.M. Distinct molecular programs regulate synapse specificity in cortical inhibitory circuits Science 2019 363 413 417 10.1126/science.aau8977 30679375 · DOI
- [158]Loh K.H. Stawski P.S. Draycott A.S. Udeshi N.D. Lehrman E.K. Wilton D.K. Svinkina T. Deerinck T.J. Ellisman M.H. Stevens B. Proteomic analysis of unbounded cellular compartments: Synaptic clefts Cell 2016 166 1295 1307.e1221 10.1016/j.cell.2016.07.041 27565350 PMC5167540 · DOI · Paper page
- [161]Lensjo K.K. Lepperod M.E. Dick G. Hafting T. Fyhn M. Removal of perineuronal nets unlocks juvenile plasticity through network mechanisms of decreased inhibition and increased gamma activity J. Neurosci. Off. J. Soc. Neurosci. 2017 37 1269 1283 10.1523/JNEUROSCI.2504-16.2016 28039374 PMC6596863 · DOI · Paper page
- [162]Su J. Chen J. Lippold K. Monavarfeshani A. Carrillo G.L. Jenkins R. Fox M.A. Collagen-derived matricryptins promote inhibitory nerve terminal formation in the developing neocortex J. Cell Biol. 2016 212 721 736 10.1083/jcb.201509085 26975851 PMC4792079 · DOI
- [163]Wu X. Muthuchamy M. Reddy D.S. Atomic force microscopy investigations of fibronectin and alpha5beta1-integrin signaling in neuroplasticity and seizure susceptibility in experimental epilepsy Epilepsy Res. 2017 138 71 80 10.1016/j.eplepsyres.2017.10.013 29096132 · DOI
- [164]Charrier C. Machado P. Tweedie-Cullen R.Y. Rutishauser D. Mansuy I.M. Triller A. A crosstalk between beta1 and beta3 integrins controls glycine receptor and gephyrin trafficking at synapses Nat. Neurosci. 2010 13 1388 1395 10.1038/nn.2645 20935643 · DOI
- [165]Szczot M. Kisiel M. Czyzewska M.M. Mozrzymas J.W. Alpha1f64 residue at gaba(a) receptor binding site is involved in gating by influencing the receptor flipping transitions J. Neurosci. Off. J. Soc. Neurosci. 2014 34 3193 3209 10.1523/JNEUROSCI.2533-13.2014 PMC6795308 24573278 · DOI
- [166]Fanjul-Fernandez M. Folgueras A.R. Cabrera S. Lopez-Otin C. Matrix metalloproteinases: Evolution, gene regulation and functional analysis in mouse models Biochim. Biophys. Acta 2010 1803 3 19 10.1016/j.bbamcr.2009.07.004 19631700 · DOI
- [167]Yap E.-L. Pettit N.L. Davis C.P. Nagy M.A. Harmin D.A. Golden E. Dagliyan O. Lin C. Rudolph S. Sharma N. Bidirectional perisomatic inhibitory plasticity of a fos neuronal network Nature 2021 590 115 121 10.1038/s41586-020-3031-0 33299180 PMC7864877 · DOI
- [168]Leger C. Dupre N. Aligny C. Benard M. Lebon A. Henry V. Hauchecorne M. Galas L. Frebourg T. Leroux P. Glutamate controls vessel-associated migration of gaba interneurons from the pial migratory route via nmda receptors and endothelial protease activation Cell. Mol. Life Sci. Cmls 2020 77 1959 1986 10.1007/s00018-019-03248-5 31392351 PMC7229000 · DOI
- [169]Roux L. Buzsaki G. Tasks for inhibitory interneurons in intact brain circuits Neuropharmacology 2015 88 10 23 10.1016/j.neuropharm.2014.09.011 25239808 PMC4254329 · DOI · Paper page
- [170]Alaiyed S. Bozzelli P.L. Caccavano A. Wu J.Y. Conant K. Venlafaxine stimulates pnn proteolysis and mmp-9-dependent enhancement of gamma power; relevance to antidepressant efficacy J. Neurochem. 2019 148 810 821 10.1111/jnc.14671 30697747 PMC6516074 · DOI
- [172]Michaluk P. Kolodziej L. Mioduszewska B. Wilczynski G.M. Dzwonek J. Jaworski J. Gorecki D.C. Ottersen O.P. Kaczmarek L. Beta-dystroglycan as a target for mmp-9, in response to enhanced neuronal activity J. Biol. Chem. 2007 282 16036 16041 10.1074/jbc.M700641200 17426029 · DOI
- [173]Waite A. Brown S.C. Blake D.J. The dystrophin-glycoprotein complex in brain development and disease Trends Neurosci. 2012 35 487 496 10.1016/j.tins.2012.04.004 22626542 · DOI
- [174]Panzanelli P. Gunn B.G. Schlatter M.C. Benke D. Tyagarajan S.K. Scheiffele P. Belelli D. Lambert J.J. Rudolph U. Fritschy J.M. Distinct mechanisms regulate gabaa receptor and gephyrin clustering at perisomatic and axo-axonic synapses on ca1 pyramidal cells J. Physiol. 2011 589 4959 4980 10.1113/jphysiol.2011.216028 21825022 PMC3224886 · DOI
- [175]Fruh S. Romanos J. Panzanelli P. Burgisser D. Tyagarajan S.K. Campbell K.P. Santello M. Fritschy J.M. Neuronal dystroglycan is necessary for formation and maintenance of functional cck-positive basket cell terminals on pyramidal cells J. Neurosci. Off. J. Soc. Neurosci. 2016 36 10296 10313 10.1523/JNEUROSCI.1823-16.2016 27707967 PMC6705590 · DOI
- [176]Pribiag H. Peng H. Shah W.A. Stellwagen D. Carbonetto S. Dystroglycan mediates homeostatic synaptic plasticity at gabaergic synapses Proc. Natl. Acad. Sci. USA 2014 111 6810 6815 10.1073/pnas.1321774111 24753587 PMC4020085 · DOI
- [177]Vaillend C. Billard J.M. Facilitated ca1 hippocampal synaptic plasticity in dystrophin-deficient mice: Role for gabaa receptors? Hippocampus 2002 12 713 717 10.1002/hipo.10068 12542223 · DOI
- [178]Gawlak M. Gorkiewicz T. Gorlewicz A. Konopacki F.A. Kaczmarek L. Wilczynski G.M. High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses Neuroscience 2009 158 167 176 10.1016/j.neuroscience.2008.05.045 18588950 · DOI · Paper page
- [179]Murase S. Lantz C.L. Kim E. Gupta N. Higgins R. Stopfer M. Hoffman D.A. Quinlan E.M. Matrix metalloproteinase-9 regulates neuronal circuit development and excitability Mol. Neurobiol. 2016 53 3477 3493 10.1007/s12035-015-9295-y 26093382 PMC4686372 · DOI · Paper page
- [180]Porcher C. Medina I. Gaiarsa J.-L. Mechanism of bdnf modulation in gabaergic synaptic transmission in healthy and disease brains Front. Cell. Neurosci. 2018 12 273 10.3389/fncel.2018.00273 30210299 PMC6121065 · DOI
- [181]Suzuki K. Hayashi Y. Nakahara S. Kumazaki H. Prox J. Horiuchi K. Zeng M. Tanimura S. Nishiyama Y. Osawa S. Activity-dependent proteolytic cleavage of neuroligin-1 Neuron 2012 76 410 422 10.1016/j.neuron.2012.10.003 23083742 · DOI
- [182]Allen M. Ghosh S. Ahern G.P. Villapol S. Maguire-Zeiss K.A. Conant K. Protease induced plasticity: Matrix metalloproteinase-1 promotes neurostructural changes through activation of protease activated receptor 1 Sci. Rep. 2016 6 35497 10.1038/srep35497 27762280 PMC5071868 · DOI
- [183]Hashimotodani Y. Ohno-Shosaku T. Yamazaki M. Sakimura K. Kano M. Neuronal protease-activated receptor 1 drives synaptic retrograde signaling mediated by the endocannabinoid 2-arachidonoylglycerol J. Neurosci. Off. J. Soc. Neurosci. 2011 31 3104 3109 10.1523/JNEUROSCI.6000-10.2011 PMC6623775 21414931 · DOI
- [184]Al-muhtasib N. Forcelli P.A. Conant K.E. Vicini S. Mmp-1 overexpression selectively alters inhibition in d1 spiny projection neurons in the mouse nucleus accumbens core Sci. Rep. 2018 8 16230 10.1038/s41598-018-34551-z 30385861 PMC6212422 · DOI
- [185]Oh S.J. Lee C.J. Distribution and function of the bestrophin-1 (best1) channel in the brain Exp. Neurobiol. 2017 26 113 121 10.5607/en.2017.26.3.113 28680296 PMC5491579 · DOI
- [187]Dembitskaya Y. Wu Y.W. Semyanov A. Tonic gaba(a) conductance favors spike-timing-dependent over theta-burst-induced long-term potentiation in the hippocampus J. Neurosci. Off. J. Soc. Neurosci. 2020 40 4266 4276 10.1523/JNEUROSCI.2118-19.2020 PMC7252479 32327534 · DOI
- [188]Bryson A. Hatch R.J. Zandt B.J. Rossert C. Berkovic S.F. Reid C.A. Grayden D.B. Hill S.L. Petrou S. Gaba-mediated tonic inhibition differentially modulates gain in functional subtypes of cortical interneurons Proc. Natl. Acad. Sci. USA 2020 117 3192 3202 10.1073/pnas.1906369117 31974304 PMC7022204 · DOI
- [189]Lepeta K. Kaczmarek L. Matrix metalloproteinase-9 as a novel player in synaptic plasticity and schizophrenia Schizophr. Bull. 2015 41 1003 1009 10.1093/schbul/sbv036 25837304 PMC4535641 · DOI
- [190]Lukasiuk K. Wilczynski G.M. Kaczmarek L. Extracellular proteases in epilepsy Epilepsy Res. 2011 96 191 206 10.1016/j.eplepsyres.2011.08.002 21893397 · DOI
- [191]Pitkanen A. Ndode-Ekane X.E. Lukasiuk K. Wilczynski G.M. Dityatev A. Walker M.C. Chabrol E. Dedeurwaerdere S. Vazquez N. Powell E.M. Neural ecm and epilepsy Prog. Brain Res. 2014 214 229 262 25410361
- [192]Stefanelli T. Bertollini C. Luscher C. Muller D. Mendez P. Hippocampal somatostatin interneurons control the size of neuronal memory ensembles Neuron 2016 89 1074 1085 10.1016/j.neuron.2016.01.024 26875623 · DOI
Cited by
Sorted by citations
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 · see citing works
- Authors
- Wiera, G., & Mozrzymas, J. W.
- Affiliations
- Wroclaw Medical University (PL)
- Corresponding author
- Wiera, Grzegorz
- Mozrzymas, Jerzy W.
- Venue
- Cells
- Publisher
- MDPI AG
- Published
- 2021-08-11
- Volume
- 10
- Issue
- 8
- Pages
- 2055
- ISSN
- 2073-4409 (ISSN-L)
- PMC
- PMC8391609
- OpenAlex
- W3188492738
- Cited by
- 36
- References
- 26
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 4 · 2023: 6 · 2022: 9
- FWCI
- 0.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cells (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Narodowe Centrum Nauki (2017/26/D/NZ4/00450, 2018/31/B/NZ4/01998)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- extracellular matrix metalloproteinases, synaptic plasticity, excitatory synapses, inhibitory synapses, long-term potentiation, MMP-9, MMP-3, synaptic proteome, extracellular proteolysis, L-type calcium channels, learning and memory, schizophrenia, mental illness, learning deficits
- MeSH terms
- Animals, gamma-Aminobutyric Acid, Humans, Learning, Neural Inhibition, Neuronal Plasticity, Synapses, Long-Term Potentiation, Matrix Metalloproteinases, Proteolysis
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