Maintenance of long-term potentiation in hippocampal mossy fiber-CA3 pathway requires fine-tuned MMP-9 proteolytic activity
Abstract
Mechanisms of synaptic plasticity involve proteolytic activity mediated by a complex system of proteases, including members of metalloproteinase (MMP) family. In particular, MMP-9 is critical in LTP maintenance in the Schaffer collateral-CA1 pathway and in the acquisition of hippocampus-dependent memory. Recent studies from this laboratory revealed that in the mossy fiber-CA3 (MF-CA3) projection, where LTP induction and expression are largely presynaptic, MMPs blockade disrupts LTP maintenance and that LTP induction is associated with increased MMP-9 expression. Here we used acute brain slices from MMP-9 knock-out mice and transgenic rats overexpressing MMP-9 to determine how manipulations in endogenous MMP-9 affect LTP in the MF-CA3 projection. Both types of transgenic models showed a normal basal synaptic transmission and short-term plasticity. Interestingly, the maintenance of LTP induced in slices from knock-out mice and overexpressing rats was nearly abolished. However, in the presence of active MMP-9, a gradual fEPSP autopotentiation was observed and tetanization evoked a marked LTP in knock-out mice. Additionally, in MMP-9-treated slices from wild-type mice, fEPSP autopotentiation also occurred and partially occluded LTP. This indicates that exogenous protease can restore LTP in null mice whereas in the wild-type, MMP-9 excess impairs LTP. We expected that LTP maintenance in transgenic rats could be re-established by a partial MMP blockade but non-saturating concentrations of MMP inhibitor were ineffective. In conclusion, we demonstrate that LTP maintenance in MF-CA3 pathway requires fine-tuned MMP-9 activity and raises the possibility that altered MMP-9 level might be detrimental for cognitive processes as observed in some neuropathologies.
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Enhanced neural activity in the hippocampus increases the active form of MMP9 into the perisynaptic space.
“Enhanced neural activity in the hippocampus increases the active form of MMP9 into the perisynaptic space (Bozdagi et al., 2007; Nagy et al., 2006; Wiera et al., 2013).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Wiera et al., 2013
MMP9 is involved in hippocampal synaptic plasticity.
“One of the most widely studied MMPs in the adult hippocampus, MMP9, is involved in hippocampal synaptic plasticity.”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Wiera et al., 2013
Cites
Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., & Werb, Z. (1998) · Cell · doi:10.1016/s0092-8674(00)81169-1 · Cited by 1,737 · see citing works
Synaptic plasticity at hippocampal mossy fibre synapses
Nicoll, R. A., & Schmitz, D. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1786 · Cited by 653 · see citing works
Unraveling mechanisms of homeostatic synaptic plasticity
Pozo, K., & Goda, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.028 · Cited by 565 · see citing works
Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity
Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2338 · Cited by 554 · see citing works
Bauvois, B. (2011) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2011.10.001 · Cited by 543 · see citing works
Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., Costa, R. M., Silva, A. J., Kaczmarek, L., & Huntley, G. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4359-05.2006 · Cited by 499 · see citing works
Bilousova, T. V., Dansie, L., Ngo, M., Aye, J., Charles, J. R., Ethell, D. W., & Ethell, I. M. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2008.061796 · Cited by 465 · see citing works
Cyclic AMP Mediates a Presynaptic Form of LTP at Cerebellar Parallel Fiber Synapses
Salin, P. A., Malenka, R. C., & Nicoll, R. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80099-9 · Cited by 439 · see citing works
Cauwe, B., den Steen, P. E. V., & Opdenakker, G. (2007) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230701340019 · Cited by 384 · see citing works
Matrix metalloproteinases in brain development and remodeling: Synaptic functions and targets
Ethell, I. M., & Ethell, D. W. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21273 · Cited by 378 · see citing works
Rab3A is essential for mossy fibre long-term potentiation in the hippocampus
Castillo, P. E., Janz, R., Sdhof, T. C., Tzounopoulos, T., Malenka, R. C., & Nicoll, R. A. (1997) · Nature · doi:10.1038/41574 · Cited by 356 · see citing works
Domenici, E., Willé, D. R., Tozzi, F., Prokopenko, I., Miller, S. L., McKeown, A., Brittain, C. F., Rujescu, D., Giegling, I., Turck, C. W., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009166 · Cited by 347 · see citing works
Wang, 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
Cauwe, B., & Opdenakker, G. (2010) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2010.501783 · Cited by 296 · see citing works
Important role of matrix metalloproteinase 9 in epileptogenesis
Wilczynski, G. M., Konopacki, F. A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P., Wawrzyniak, M., Malinowska, M., Okulski, P., Kolodziej, L. R., et al. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200708213 · Cited by 292 · see citing works
Learning-related feedforward inhibitory connectivity growth required for memory precision
Ruediger, S., Vittori, C. G., Bednarek, E., Genoud, C., Strata, P., Sacchetti, B., & Caroni, P. (2011) · Nature · doi:10.1038/nature09946 · Cited by 282 · see citing works
Meighan, S. E., Meighan, P. C., Choudhury, P., Davis, C. J., Olson, M. L., Zornes, P. A., Wright, J. W., & Harding, J. W. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03565.x · Cited by 281 · see citing works
Matrix metalloproteinase proteomics: substrates, targets, and therapy
Morrison, C., Butler, G. S., Rodrı́guez, D., & Overall, C. M. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.06.006 · Cited by 266 · see citing works
Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP
Contractor, A., Rogers, C., Maron, C., Henkemeyer, M. J., Swanson, G. T., & Heinemann, S. F. (2002) · Science · doi:10.1126/science.1069081 · Cited by 262 · see citing works
Metzincin Proteases and Their Inhibitors: Foes or Friends in Nervous System Physiology?
Rivera, S., Khrestchatisky, M., Kaczmarek, L., Rosenberg, G. A., & Jaworski, D. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3467-10.2010 · Cited by 237 · see citing works
Transmembrane collagen XVII, an epithelial adhesion protein, is shed from the cell surface by ADAMs
Franzke, C.-W., Tasanen, K., Schäcke, H., Zhou, Z., Tryggvason, K., Mauch, C., Zigrino, P., Sunnarborg, S. W., Lee, D. C., Fahrenholz, F., et al. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf532 · Cited by 230 · 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-citationNeuropsin cleaves EphB2 in the amygdala to control anxiety
Attwood, B. K., Bourgognon, J.-M., Patel, S., Mucha, M. W., Schiavon, E., Skrzypiec, A. E., Young, K. W., Shiosaka, S., Korostyński, M., Piechota, M., et al. (2011) · Nature · doi:10.1038/nature09938 · Cited by 200 · see citing works
Bozdagi, O., Nagy, V., Kwei, K. T., & Huntley, G. W. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00202.2007 · Cited by 182 · see citing works
Structural Contributions to Short-Term Synaptic Plasticity
Xu‐Friedman, M. A., & Regehr, W. G. (2004) · Physiological Reviews · doi:10.1152/physrev.00016.2003 · Cited by 178 · see citing works
Kramár, E. A., Lin, B., Lin, C., Arai, A., Gall, C. M., & LYNCH, G. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0800-04.2004 · Cited by 177 · see citing works
Xavier, G. F., Oliveira-Filho, F. J. B., & Santos, A. M. G. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:6 · Cited by 175 · see citing works
Dystroglycan distribution in adult mouse brain: a light and electron microscopy study
Zaccaria, M. L., Tommaso, F. D., Brancaccio, A., Paggi, P., & Petrucci, T. C. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00092-6 · Cited by 168 · see citing works
Galimberti, I., Gogolla, N., Alberi, S., Santos, A. F., Müller, D., & Caroni, P. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.026 · Cited by 163 · see citing works
Increased Matrix Metalloproteinase 9 Activity in Mild Cognitive Impairment
Bruno, M. A., Mufson, E. J., Wuu, J., & Cuello, A. C. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181c22569 · Cited by 163 · see citing works
TIMP-1 Abolishes MMP-9-Dependent Long-lasting Long-term Potentiation in the Prefrontal Cortex
Okulski, P., Jay, T. M., Jaworski, J., Duniec, K., Dzwonek, J., Konopacki, F. A., Wilczynski, G. M., Sánchez‐Capelo, A., Mallet, J. J., & Kaczmarek, L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.012 · Cited by 154 · see citing works
Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity
Włodarczyk, J., Mukhina, I. V., Kaczmarek, L., & Dityatev, A. E. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20958 · Cited by 123 · see citing works
Localizing matrix metalloproteinase activities in the pericellular environment
Murphy, G., & Nagase, H. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07918.x · Cited by 117 · see citing works
Bretin, S., Reibel, S., Charrier, E., Maus, M., Auvergnon, N., Thévenoux, A., Glowinski, J., Rogemond, V., Prémont, J., Honnorat, J., et al. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20465 · Cited by 117 · see citing works
Armstrong, J. N., Saganich, M. J., Xu, N., Henkemeyer, M. J., Heinemann, S. F., & Contractor, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4338-05.2006 · Cited by 108 · see citing works
Lin, K., Sloniowski, S., Ethell, D. W., & Ethell, I. M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m804401200 · Cited by 105 · see citing works
Meighan, P. C., Meighan, S. E., Davis, C. J., Wright, J. W., & Harding, J. W. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04682.x · Cited by 95 · see citing works
Holahan, M. R., Rekart, J. L., Sandoval, J., & Routtenberg, A. (2006) · Hippocampus · doi:10.1002/hipo.20185 · Cited by 83 · see citing works
RYBAKOWSKI, J. K. (2009) · Cardiovascular Psychiatry and Neurology · doi:10.1155/2009/904836 · Cited by 82 · see citing works
Wright, J. W., & Harding, J. W. (2009) · Neural Plasticity · doi:10.1155/2009/579382 · Cited by 79 · see citing works
Inhibition of Matrix Metalloproteinases by Peptidyl Hydroxamic Acids
Odake, S., Morita, Y., Morikawa, T., Yoshida, N., Hori, H., & Nagai, Y. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.1392 · Cited by 71 · see citing works
Howell, M. D., & Gottschall, P. E. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.034 · Cited by 66 · see citing works
Enhanced neuronal plasticity and elevated endogenous sAPPα levels in mice over‐expressing MMP9
Fragkouli, A., Papatheodoropoulos, C., Georgopoulos, S., Stamatakis, A., Stylianopoulou, F., Tsilibary, E. C., & Tzinia, A. K. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07637.x · Cited by 64 · 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
Structural plasticity of hippocampal mossy fiber synapses as revealed by high‐pressure freezing
Zhao, S., Studer, D., Chai, X., Graber, W. A., Brose, N., Nestel, S., Young, C. C., Rodriguez, E., Saetzler, K., & Frotscher, M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23040 · Cited by 56 · see citing works
Wójtowicz, T., & Mozrzymas, J. W. (2010) · Hippocampus · doi:10.1002/hipo.20787 · Cited by 43 · see citing works
Bajor, 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 37 · see citing works
Dieni, S., & Rees, S. M. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10422 · Cited by 34 · see citing works
Lee, T. W., Tsang, V. W. K., & Birch, N. P. (2008) · Neuron Glia Biology · doi:10.1017/s1740925x09990172 · Cited by 30 · see citing works
Wiera, G., Wójtowicz, T., Lebida, K., Piotrowska, A., Drulis‐Fajdasz, D., Gomułkiewicz, A., de Carrillo, D. G., Podhorska‐Okołów, M., Capogna, M., Wilczynski, G. M., et al. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.04.005 · Cited by 29 · see citing works
Fisher, K. E., Fei, Q., Laird, E. R., Stock, J. L., Allen, M. R., Sahagan, B. G., & Strick, C. A. (2002) · Biochemistry · doi:10.1021/bi012076t · Cited by 20 · see citing works
Kamiya, H. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0720-12.2012 · Cited by 10 · see citing works
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Vafadari, B., Salamian, A., & Kaczmarek, L. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13415 · Cited by 381 · see citing works
Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
Reinhard, S. M., Razak, K., & Ethell, I. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00280 · Cited by 219 · see citing works
MMPs in learning and memory and neuropsychiatric disorders
Beroun, A., Mitra, S., Michaluk, P., Pijet, B., Stefaniuk, M., & Kaczmarek, L. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03180-8 · Cited by 207 · see citing works
Integrins in synapse regulation
Park, Y. K., & Goda, Y. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.138 · Cited by 167 · see citing works
Wiera, G., & Mozrzymas, J. W. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00427 · Cited by 117 · see citing works
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 · see citing works
Murase, S., Lantz, C. L., & Quinlan, E. M. (2017) · eLife · doi:10.7554/elife.27345 · Cited by 87 · see citing works
Matrix metalloproteinase-9 involvement in the structural plasticity of dendritic spines
Stawarski, M., Stefaniuk, M., & Włodarczyk, J. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00068 · Cited by 83 · see citing works
Neural ECM proteases in learning and synaptic plasticity
Tsilibary, E. C., Tzinia, A. K., Radenović, L., Stamenković, V., Lebitko, T., Mucha, M. W., Pawlak, R., Frischknecht, R., & Kaczmarek, L. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63486-3.00006-2 · Cited by 74 · see citing works
Matrix Metalloproteinase-9 as a Novel Player in Synaptic Plasticity and Schizophrenia: Table 1.
Łepeta, K., & Kaczmarek, L. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv036 · Cited by 75 · see citing works
Transient ECM protease activity promotes synaptic plasticity
Magnowska, M., Górkiewicz, T., Beroun, A., Wawrzyniak, M., Rutkowska-Włodarczyk, I., Kaczmarek, L., & Włodarczyk, J. (2016) · Scientific Reports · doi:10.1038/srep27757 · Cited by 73 · see citing works
Wiera, G., Nowak, D., Hove, I. V., Dzięgiel, P., Moons, L., & Mozrzymas, J. W. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2170-16.2016 · Cited by 53 · see citing works
Activity-controlled proteolytic cleavage at the synapse
Sonderegger, P., & Matsumoto, K. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.05.007 · Cited by 49 · see citing works
The malleable brain: plasticity of neural circuits and behavior – a review from students to students
Schaefer, N., Rotermund, C., Blumrich, E., Lourenco, M. V., Joshi, P., Hegemann, R. U., Jamwal, S., Ali, N., Romero, E. M. G., Sharma, S., et al. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14107 · Cited by 50 · see citing works
Allen, M., Ghosh, S., Ahern, G. P., Villapol, S., Maguire‐Zeiss, K. A., & Conant, K. E. (2016) · Scientific Reports · doi:10.1038/srep35497 · Cited by 49 · see citing works
Majewski, Ł., Maciąg, F., Boguszewski, P. M., Wasilewska, I., Wiera, G., Wójtowicz, T., Mozrzymas, J. W., & Kuźnicki, J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.11.025 · Cited by 43 · see citing works
Lonskaya, I., Partridge, J. G., Lalchandani, R. R., Chung, A. J., Lee, T., Vicini, S., Hoe, H.-S., Seung Taik, L. I. M., & Conant, K. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069136 · Cited by 42 · see citing works
Stefano, M. E. D., & Herrero, M. T. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.08.002 · Cited by 42 · see citing works
Xiong, G., Metheny, H. E., Johnson, B. N., & Cohen, A. S. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00107 · Cited by 40 · see citing works
Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses
Wiera, G., & Mozrzymas, J. W. (2021) · Cells · doi:10.3390/cells10082055 · Cited by 36 · see citing works
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 · see citing works
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 · see citing works
Gao, J., Yi, H., Tang, X., Feng, X., Yu, M., Sha, W., Wang, X., Zhang, X., & Zhang, X. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00646 · Cited by 36 · see citing works
Wójtowicz, T., & Mozrzymas, J. W. (2013) · Hippocampus · doi:10.1002/hipo.22205 · Cited by 34 · see citing works
A conceptualized model linking matrix metalloproteinase-9 to schizophrenia pathogenesis
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2019.12.015 · Cited by 34 · see citing works
Involvement of cellular metabolism in age-related LTP modifications in rat hippocampal slices
Drulis‐Fajdasz, D., Wójtowicz, T., Wawrzyniak, M., Włodarczyk, J., Mozrzymas, J. W., & Rakus, D. (2015) · Oncotarget · doi:10.18632/oncotarget.4188 · Cited by 32 · see citing works
Association between age‑related hearing loss and cognitive decline in C57BL/6J mice
Yang, D., Guo, C., Chen, D., Chen, S., Peng, Y., Song, H., & Shi, J. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.9118 · Cited by 30 · see citing works
Seitz‐Holland, J., Seethaler, M., Makris, N., Rushmore, J., Cho, K.-I. K., Rizzoni, E., Vangel, M. G., Şenay, O., Heller, C., Pasternak, O., et al. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-00997-5 · Cited by 27 · see citing works
Grochecki, P., Smaga, I., Łopatyńska-Mazurek, M., Gibuła‐Tarłowska, E., Kędzierska, E., Listos, J., Talarek, S., Marszałek‐Grabska, M., Hubalewska‐Mazgaj, M., Korga-Plewko, A., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020589 · Cited by 25 · see citing works
Casas, B. S., Vitória, G., Prieto, C. P., Casas, M., Chacón, C., Uhrig, M., Ezquer, F. E., Ezquer, M., Rehen, S. K., & Palma, V. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01653-0 · Cited by 25 · see citing works
Gore, S. V., James, E. J., Huang, L.-C., Park, J. J., Berghella, A. P., Thompson, A. C., Cline, H. T., & Aizenman, C. D. (2021) · eLife · doi:10.7554/elife.62147 · Cited by 24 · see citing works
Ganguly, K., Adhikary, K., Acharjee, A., Acharjee, P., Trigun, S. K., Mutlaq, A. S., Ashique, S., Yasmin, S., Alshahrani, A. M., & Ansari, M. Y. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.135967 · Cited by 23 · see citing works
Matrix metalloproteinase‐9: A magic drug target in neuropsychiatry?
Kaczmarek, K., Protokowicz, K., & Kaczmarek, L. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15976 · Cited by 23 · see citing works
Wójtowicz, T., Brzdąk, P., & Mozrzymas, J. W. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00313 · Cited by 20 · see citing works
Brzdąk, P., Nowak, D., Wiera, G., & Mozrzymas, J. W. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00178 · Cited by 21 · see citing works
Azpurua, J., Mahoney, R. E., & Eaton, B. A. (2018) · Aging Cell · doi:10.1111/acel.12729 · Cited by 20 · see citing works
Matrix metalloproteinase-3 in brain physiology and neurodegeneration
Lech, A. M., Wiera, G., & Mozrzymas, J. W. (2019) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/110319 · Cited by 22 · see citing works
Wiera, G., Szczot, M., Wójtowicz, T., Lebida, K., Koza, P., & Mozrzymas, J. W. (2015) · PubMed · Cited by 20 · see citing works
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 · see citing works
BDNF-driven synaptic plasticity requires autocrine matrix metalloproteinase–9 activity
Legutko, D., Bijoch, Ł., Olszak, G., Kuźniewska, B., Kalita, K. B., Yasuda, R., Kaczmarek, L., & Michaluk, P. (2025) · Science Advances · doi:10.1126/sciadv.adx2369 · Cited by 20 · see citing works
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 · see citing works
Liu, C. Z., Guo, D. S., Ma, J. J., Dong, L. R., Chang, Q., Yang, H. Q., Liang, K., Li, X. H., Yang, D., Fan, Y., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.889257 · Cited by 17 · see citing works
Lebida, K., & Mozrzymas, J. W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0174-y · Cited by 16 · see citing works
Amontree, M., Nelson, M., Stefansson, L., Pak, D. T. S., Maguire-Zeiss, K., Turner, R., & Conant, K. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16031 · Cited by 13 · see citing works
Li, Y., Partridge, J. G., Berger, C., Sepulveda‐Rodriguez, A., Vicini, S., & Conant, K. E. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13146 · Cited by 11 · see citing works
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Salamian, A., Legutko, D., Nowicka, K., Badyra, B., Kaźmierska, P., Caban, B., Kowalczyk, T., Kaczmarek, L., & Beroun, A. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab050 · Cited by 8 · see citing works
Matrix Metalloproteinase 9 (MMP-9) in Learning and Memory
Knapska, E., & Kaczmarek, L. (2015) · Springer eBooks · doi:10.1007/978-3-319-24364-1_9 · Cited by 6 · see citing works
The Molecular Basis of Destabilization of Synapses as a Factor of Structural Plasticity
Kudryashova, I. V. (2019) · Neurochemical Journal · doi:10.1134/s1819712419010136 · Cited by 4 · see citing works
Virtuoso, A., Galanis, C., Lenz, M., Papa, M., & Vlachos, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042346 · Cited by 3 · see citing works
MMP-9 plasma level as biomarker of cochlear implantation outcome in cohort study of deaf children
Matusiak, M., Oziębło, D., Ołdak, M., Rejmak, E., Kaczmarek, L., Dobek, D., & Skarżyńśki, H. (2023) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-023-07924-y · Cited by 2 · see citing works
Olson, M. L., Badenoch, B., Blatti, M., Buching, C., & Glewwe, N. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114460 · Cited by 2 · see citing works
Virtuoso, A., Galanis, C., Lenz, M., Papa, M., & Vlachos, A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.10.575060 · Cited by 1 · see citing works
NEUROTROPHIN-CHEMOKINE RECEPTOR INTERACTIONS ON MACROPHAGES REGULATE HIV NEUROPATHOGENESIS
Williams, K. S. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/3af8-4p67
MOLEKULAAR- JA RAKUBIOLOOGIA INSTITUUT
Ülikool, T. R., Pajo, K., & Klaas, M. (2015)
Allen, M. (2017) · DigitalGeorgetown (Georgetown University Library)
Chen, Z., Wang, X., & Han, F. (2025) · Scientific Reports · doi:10.1038/s41598-025-28204-1
- Authors
- Wiera, G., Wozniak, G., Bajor, M., Kaczmarek, L., & Mozrzymas, J. W.
- Affiliations
- University of Wrocław (PL)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Wroclaw Medical University (PL)
- Corresponding author
- Wiera, Grzegorz
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2013-04-05
- Volume
- 23
- Issue
- 6
- Pages
- 529-543
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2052724410
- Cited by
- 57
- References
- 52
- Citations by year
- 2025: 2 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 1 · 2019: 5 · 2018: 4 · 2017: 7 · 2016: 7 · 2015: 10 · 2014: 5 · 2013: 2
- FWCI
- 3.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- long-term potentiation, LTP maintenance, MMP-9, metalloproteinases, synaptic plasticity, presynaptic plasticity, tetanic potentiation, MMP-9 knockout mice, proteolytic activity
- MeSH terms
- Animals, Enzyme Activation, Male, Mice, Inbred C57BL, Neural Pathways, Organ Culture Techniques, Rats, Wistar, Long-Term Potentiation, Mice, Knockout, Mossy Fibers, Hippocampal, Matrix Metalloproteinase 9, Mice, Rats, Rats, Transgenic, CA3 Region, Hippocampal, Proteolysis
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