A delicate balance: role of MMP-9 in brain development and pathophysiology of neurodevelopmental disorders.
Open accessAbstract
The extracellular matrix (ECM) is a critical regulator of neural network development and plasticity. As neuronal circuits develop, the ECM stabilizes synaptic contacts, while its cleavage has both permissive and active roles in the regulation of plasticity. Matrix metalloproteinase 9 (MMP-9) is a member of a large family of zinc-dependent endopeptidases that can cleave ECM and several cell surface receptors allowing for synaptic and circuit level reorganization. It is becoming increasingly clear that the regulated activity of MMP-9 is critical for central nervous system (CNS) development. In particular, MMP-9 has a role in the development of sensory circuits during early postnatal periods, called 'critical periods.' MMP-9 can regulate sensory-mediated, local circuit reorganization through its ability to control synaptogenesis, axonal pathfinding and myelination. Although activity-dependent activation of MMP-9 at specific synapses plays an important role in multiple plasticity mechanisms throughout the CNS, misregulated activation of the enzyme is implicated in a number of neurodegenerative disorders, including traumatic brain injury, multiple sclerosis, and Alzheimer's disease. Growing evidence also suggests a role for MMP-9 in the pathophysiology of neurodevelopmental disorders including Fragile X Syndrome. This review outlines the various actions of MMP-9 during postnatal brain development, critical for future studies exploring novel therapeutic strategies for neurodevelopmental disorders.
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?
MMP-9 is a zinc-dependent endopeptidase expressed in various cells within the CNS which is capable of cleaving ECM proteins, including collagen and laminin.
“MMP-9 is a zinc-dependent endopeptidase expressed in various cells within the CNS which is capable of cleaving ECM proteins, including collagen and laminin (reviewed in Reinhard et al., 2015).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Reinhard et al., 2015
Peak MMP-9 expression is observed during postnatal development and is reduced during adulthood.
“Peak MMP-9 expression is observed during postnatal development and is reduced during adulthood (Bednarek et al., 2009; Reinhard et al., 2015; Wen et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Reinhard et al., 2015
Removal of MMP-9 in Mmp9 KO mice mostly did not affect auditory ERP N1 amplitude or habituation, although MMP-9 is involved in sensory system development (Reinhard et al., 2015).
“Although MMP-9 is involved in sensory system development (reviewed in Reinhard et al., 2015), we found that auditory ERP N1 amplitude and habituation are mostly unaffected by the removal of MMP-9 (Mmp9 KO mice).”
From Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome (2016) · cites this paper as Reinhard et al., 2015
A significant reduction in parvalbumin expression and parvalbumin/perineuronal net colocalization in MMP-9 knockout mice is consistent with the role of MMP-9 in neurodevelopment, suggesting that too much or too little MMP-9 would affect parvalbumin cell development.
“In addition, we found a significant reduction in PV expression and PV/PNN colocalization in MMP-9 -/mice (not shown), which is consistent with MMP-9 role in neurodevelopment (reviewed in Reinhard et al. 2015), suggesting that too much or too little MMP-9 would affect PV cell development.”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Reinhard et al. 2015
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
RGD AND OTHER RECOGNITION SEQUENCES FOR INTEGRINS
Ruoslahti, E. (1996) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.12.1.697 · Cited by 3,191 · see citing works
Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected
Santos, S. E. D., Porfírio, J., Cunha, F., Manger, P. R., Tavares, W. C., Pessôa, L. M., Raghanti, M. A., Sherwood, C. C., & Herculano‐Houzel, S. (2017) · Brain Behavior and Evolution · doi:10.1159/000452856 · Cited by 2,651 · see citing works
Chondroitinase ABC promotes functional recovery after spinal cord injury
Bradbury, E. J., Moon, L. D. F., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., Fawcett, J. W., & McMahon, S. B. (2002) · Nature · doi:10.1038/416636a · Cited by 2,357 · see citing works
Azevedo, F. A. C., Carvalho, L. R. B., Grinberg, L. T., Farfel, J. M., Ferretti, R. E. L., Leite, R. E. P., Filho, W. J., Lent, R., & Herculano‐Houzel, S. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21974 · Cited by 2,337 · see citing works
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323 · see citing works
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679 · see citing works
MMP-9 Supplied by Bone Marrow–Derived Cells Contributes to Skin Carcinogenesis
Coussens, L. M., Tinkle, C. L., Hanahan, D., & Werb, Z. (2000) · Cell · doi:10.1016/s0092-8674(00)00139-2 · Cited by 1,306 · see citing works
Hensch, T. K. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144327 · Cited by 1,300 · see citing works
Altman, J. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450402 · Cited by 996 · see citing works
Biochemistry and Molecular Biology of Gelatinase B or Matrix Metalloproteinase-9 (MMP-9)
den Steen, P. E. V., Dubois, B., Nelissen, I., Rudd, P., Dwek, R., & Opdenakker, G. (2002) · Critical reviews in biochemistry and molecular biology · doi:10.1080/10409230290771546 · Cited by 948 · see citing works
Extracellular space structure revealed by diffusion analysis
Nicholson, C., & Syková, E. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01261-2 · Cited by 914 · see citing works
Bayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900107 · Cited by 913 · see citing works
Altman, J. (1972) · The Journal of Comparative Neurology · doi:10.1002/cne.901450305 · Cited by 912 · see citing works
GSK-3β Regulates Phosphorylation of CRMP-2 and Neuronal Polarity
Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., & Kaibuchi, K. (2005) · Cell · doi:10.1016/j.cell.2004.11.012 · Cited by 877 · see citing works
Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse
Gordon, J. A., & Stryker, M. P. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03274.1996 · Cited by 856 · see citing works
The oligodendrocyte and its many cellular processes
Pfeiffer, S. E., Warrington, A. E., & Bansal, R. (1993) · Trends in Cell Biology · doi:10.1016/0962-8924(93)90213-k · Cited by 852 · see citing works
Response properties of vibrissa units in rat SI somatosensory neocortex
Simons, D. J. (1978) · Journal of Neurophysiology · doi:10.1152/jn.1978.41.3.798 · Cited by 771 · see citing works
CRMP-2 binds to tubulin heterodimers to promote microtubule assembly
Fukata, Y., Itoh, T. J., Kimura, T., Ménager, C., Nishimura, T., Shiromizu, T., Watanabe, H., Inagaki, N., Iwamatsu, A., Hotani, H., et al. (2002) · Nature Cell Biology · doi:10.1038/ncb825 · Cited by 761 · see citing works
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L., & Maffei, L. (1994) · Vision Research · doi:10.1016/0042-6989(94)90210-0 · Cited by 656 · see citing works
Metalloproteinases: Mediators of Pathology and Regeneration in the CNS
Yong, V. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1807 · Cited by 582 · see citing works
The dual role of the extracellular matrix in synaptic plasticity and homeostasis
Dityatev, A., Schachner, M., & Sonderegger, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2898 · Cited by 559 · see citing works
Stevens (2002) · doi:10.1016/s0896-6273(02)01067-x · Cited by 543 · see citing works
Harris, E. W., & Cotman, C. W. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90451-9 · Cited by 540 · 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
NMDA Receptor-Dependent Ocular Dominance Plasticity in Adult Visual Cortex
Sawtell, N. B., Frenkel, M. Y., Philpot, B. D., Nakazawa, K., Tonegawa, S., & Bear, M. F. (2003) · Neuron · doi:10.1016/s0896-6273(03)00323-4 · Cited by 482 · see citing works
Ruoslahti, E. (1996) · Glycobiology · doi:10.1093/glycob/6.5.489 · Cited by 467 · 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
Self-citationFlow of excitation within rat barrel cortex on striking a single vibrissa
Armstrong‐James, M., Fox, K. D., & Das-Gupta, A. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.4.1345 · Cited by 426 · see citing works
A critical period for experience-dependent synaptic plasticity in rat barrel cortex
Fox, K. D. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-05-01826.1992 · Cited by 420 · see citing works
Critical Period Window for Spectral Tuning Defined in the Primary Auditory Cortex (A1) in the Rat
de Villers‐Sidani, E., Chang, E. F., Bao, S., & Merzenich, M. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3227-06.2007 · Cited by 378 · 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
Self-citationStructural and functional recovery from early monocular deprivation in adult rats
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N., & Maffei, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602657103 · Cited by 367 · 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
Development and critical period plasticity of the barrel cortex
Erzurumlu, R. S., & Gaspar, P. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08075.x · Cited by 344 · see citing works
Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages
Woolsey, T. A., & Wann, J. R. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901700105 · Cited by 328 · 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
The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus
Ribak, C. E., Seress, L., & Amaral, D. G. (1985) · Journal of Neurocytology · doi:10.1007/bf01170832 · Cited by 311 · see citing works
Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex
Fox, K. D. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00027-1 · Cited by 307 · see citing works
Excitatory neuronal connectivity in the barrel cortex
Feldmeyer, D. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00024 · Cited by 298 · see citing works
Leigh, M. J. S., Nguyen, D. V., Mu, Y., Winarni, T. I., Schneider, A., Chechi, T., Polussa, J., Doucet, P., Tassone, F., Rivera, S. M., et al. (2013) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e318287cd17 · Cited by 298 · 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
Development of the Nervous System
(2019) · Elsevier eBooks · doi:10.1016/c2014-0-01601-2 · Cited by 281 · see citing works
MMPs as therapeutic targets—Still a viable option?
Fingleton, B. (2007) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2007.06.006 · Cited by 280 · see citing works
Sensory Deprivation Alters Aggrecan and Perineuronal Net Expression in the Mouse Barrel Cortex
McRae, P. A., Rocco, M. M., Kelly, G., Brumberg, J. C., & Matthews, R. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5425-06.2007 · Cited by 272 · see citing works
Disruption of primary auditory cortex by synchronous auditory inputs during a critical period
Zhang, L. I., Bao, S., & Merzenich, M. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261707398 · Cited by 270 · see citing works
Matrix Metalloproteinase-9/Gelatinase B Is Required for Process Outgrowth by Oligodendrocytes
Oh, L. Y. S., Larsen, P. H., Krekoski, C. A., Edwards, D. R., Donovan, F. M., Werb, Z., & Yong, V. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08464.1999 · Cited by 267 · see citing works
Ye, P., Carson, J. L., & D'Ercole, A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07344.1995 · Cited by 266 · see citing works
Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain
Dzwonek, J., Rylski, M., & Kaczmarek, L. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.03.070 · Cited by 256 · see citing works
A critical period for auditory thalamocortical connectivity
Barkat, T. R., Polley, D. B., & Hensch, T. K. (2011) · Nature Neuroscience · doi:10.1038/nn.2882 · Cited by 252 · see citing works
Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene
Foran, D., & Peterson, A. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04890.1992 · Cited by 250 · see citing works
Matthews, M. A., & Duncan, D. (1971) · The Journal of Comparative Neurology · doi:10.1002/cne.901420102 · Cited by 241 · see citing works
Transsynaptic Signaling by Activity-Dependent Cleavage of Neuroligin-1
Peixoto, R. T., Kunz, P. A., Kwon, H., Mabb, A. M., Sabatini, B. L., Philpot, B. D., & Ehlers, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.006 · Cited by 224 · see citing works
Open-label add-on treatment trial of minocycline in fragile X syndrome.
Paribello, C., Tao, L., Folino, A., Berry-Kravis, E., Tranfaglia, M., Ethell, I. M., & Ethell, D. W. (2010) · BMC Neurology · doi:10.1186/1471-2377-10-91 · Cited by 223 · see citing works
Self-citationInfluence 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
Matrix Metalloproteinase-9 Controls NMDA Receptor Surface Diffusion through Integrin β1 Signaling
Michaluk, P., Mikasová, L., Groc, L., Frischknecht, R., Choquet, D., & Kaczmarek, L. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5346-08.2009 · Cited by 204 · see citing works
Gkogkas, 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
Shi, Y., & Ethell, I. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4091-05.2006 · Cited by 200 · see citing works
Self-citationMizoguchi, H., Nakade, J., Tachibana, M., Ibi, D., Someya, E., Koike, H., Kamei, H., Nabeshima, T., Itohara, S., Takuma, K., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3118-11.2011 · Cited by 199 · see citing works
Minocycline for Short‐Term Neuroprotection
Elewa, H. F., Hilali, H., Hess, D. C., Machado, L. S., & Fagan, S. C. (2006) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1592/phco.26.4.515 · Cited by 198 · see citing works
Vaillant, C., Didier‐Bazès, M., Hutter, A., Belin, M., & Thomasset, N. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-12-04994.1999 · Cited by 188 · 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
Modulation of Perineuronal Nets and Parvalbumin with Developmental Song Learning
Balmer, T. S., Carels, V. M., Frisch, J. L., & Nick, T. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2974-09.2009 · Cited by 181 · see citing works
Genersch, E., Hayeß, K., Wefeld‐Neuenfeld, Y., & Haller, H. G. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.23.4319 · Cited by 178 · see citing works
Nikodémová, M., Duncan, I. D., & Watters, J. J. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03520.x · Cited by 176 · see citing works
Tian, L., Stefanidakis, M., Lin, N., Lint, P. V., Nyman-Huttunen, H., Libert, C., Itohara, S., Mishina, M., Rauvala, H., & Gahmberg, C. G. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200612097 · Cited by 173 · see citing works
Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures
Richards, D. A., Mateos, J. M., Hugel, S., de Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501881102 · Cited by 161 · see citing works
High MMP-9 activity levels in fragile X syndrome are lowered by minocycline
Dziembowska, M., Pretto, D. I., Janusz, A., Kaczmarek, L., Leigh, M. J., Gabriel, N., Durbin‐Johnson, B., Hagerman, R. J., & Tassone, F. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.36023 · Cited by 161 · see citing works
Ferguson, T. A., & Muir, D. (2000) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2000.0859 · Cited by 160 · see citing works
Sidhu, H., Dansie, L. E., Hickmott, P. W., Ethell, D. W., & Ethell, I. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1162-14.2014 · Cited by 155 · see citing works
Self-citationTIMP-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
Stage-Specific Action of Matrix Metalloproteinases Influences Progressive Hereditary Kidney Disease
Zeisberg, M., Khurana, M., Rao, V. H., Cosgrove, D. E., Rougier, J., Werner, M. C., Shield, C. F., Werb, Z., & Kalluri, R. (2006) · PLoS Medicine · doi:10.1371/journal.pmed.0030100 · Cited by 154 · see citing works
Proper, E. A., Oestreicher, A. B., Jansen, G. H., Veelen, C. W. M. V., van Rijen, P. C., Gispen, W. H., & Graan, P. N. E. D. (2000) · Brain · doi:10.1093/brain/123.1.19 · Cited by 152 · see citing works
Uhm, J. H., Dooley, N. P., Oh, L. Y. S., & Yong, V. W. (1998) · Glia · doi:10.1002/(sici)1098-1136(199801)22:1 · Cited by 144 · see citing works
Altered auditory processing in a mouse model of fragile X syndrome
Rotschafer, S. E., & Razak, K. A. (2013) · Brain Research · doi:10.1016/j.brainres.2013.02.038 · Cited by 138 · see citing works
Self-citationLarsen, P. H., DaSilva, A. G., Conant, K. E., & Yong, V. W. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1880-05.2006 · Cited by 138 · see citing works
MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum
Vaillant, C. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00196-9 · Cited by 135 · see citing works
Effects of monocular deprivation in kittens
Hubel, D. H., & Wiesel, T. N. (1964) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00348878 · Cited by 132 · see citing works
Rotschafer, S. E., Trujillo, M. S., Dansie, L. E., Ethell, I. M., & Razak, K. A. (2012) · Brain Research · doi:10.1016/j.brainres.2011.12.041 · Cited by 130 · see citing works
Self-citationKossut, M. M., Hand, P. J., Greenberg, J. H., & Hand, C. L. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.2.829 · Cited by 129 · see citing works
Activity-Dependent Local Translation of Matrix Metalloproteinase-9
Dziembowska, M., Miłek, J., Janusz, A., Rejmak, E., Romanowska, E., Górkiewicz, T., Tiron, A., Bramham, C. R., & Kaczmarek, L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6028-11.2012 · Cited by 127 · see citing works
Bernard‐Trifilo, J. A., Kramár, E. A., Torp, R., Lin, C., Pineda, E. A., LYNCH, G. S., & Gall, C. M. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03062.x · Cited by 120 · see citing works
Steward, O., & Falk, P. M. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903140311 · Cited by 114 · see citing works
Hashimoto, K., & Kano, M. (2005) · Neuroscience Research · doi:10.1016/j.neures.2005.07.007 · Cited by 113 · see citing works
The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses.
Janusz, A., Miłek, J., Perycz, M., Pacini, L., Bagni, C., Kaczmarek, L., & Dziembowska, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2207-13.2013 · Cited by 112 · see citing works
Electrocortical changes associated with minocycline treatment in fragile X syndrome
Schneider, A., Leigh, M. J., Adams, P., Nanakul, R., Chechi, T., Olichney, J., Hagerman, R., & Hessl, D. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113494105 · Cited by 108 · see citing works
Utari, A., Chonchaiya, W., Rivera, S. M., Schneider, A., Hagerman, R. J., Faradz, S. M. H., Ethell, I. M., & Nguyen, D. V. (2010) · American Journal on Intellectual and Developmental Disabilities · doi:10.1352/1944-7558-115.5.433 · Cited by 105 · see citing works
Self-citationLin, 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
Self-citationAuditory Processing in Fragile X Syndrome
Rotschafer, S. E., & Razak, K. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00019 · Cited by 103 · see citing works
Self-citationEsparza, J., Kruse, M., Lee, J. Y., Michaud, M., & Madri, J. A. (2004) · The FASEB Journal · doi:10.1096/fj.04-2445com · Cited by 103 · see citing works
Ahmed, Z., Dent, R. G., Leadbeater, W. E., Smith, C., Berry, M., & Logan, A. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.08.013 · Cited by 102 · see citing works
Gawlak, M., Górkiewicz, T., Gorlewicz, A., Konopacki, F. A., Kaczmarek, L., & Wilczynski, G. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.045 · Cited by 101 · see citing works
Yamamori, H., Hashimoto, R., Ishima, T., Kishi, F., Yasuda, Y., Ohi, K., Fujimoto, M., Umeda-Yano, S., Ito, A., Hashimoto, K., et al. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.09.059 · Cited by 101 · see citing works
Chattopadhyay, S., & Shubayev, V. I. (2009) · Glia · doi:10.1002/glia.20851 · Cited by 101 · see citing works
Long-lasting effects of minocycline on behavior in young but not adult Fragile X mice.
Dansie, L. E., Phommahaxay, K., Okusanya, A. G., Uwadia, J., Huang, M., Rotschafer, S. E., Razak, K. A., Ethell, D. W., & Ethell, I. M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.04.058 · Cited by 95 · see citing works
Self-citationMaravall, M., Stern, E. A., & Svoboda, K. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00598.2003 · Cited by 95 · see citing works
A precritical period for plasticity in visual cortex
Feller, M. B., & Scanziani, M. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.01.012 · Cited by 92 · see citing works
Kelly, M. K., Carvell, G. E., Kodger, J. M., & Simons, D. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09117.1999 · Cited by 88 · see citing works
RYBAKOWSKI, J. K., Remlinger-Molenda, A., Czech-Kucharska, A., Wójcicka, M., Michalak, M., & Losy, J. (2012) · Journal of Affective Disorders · doi:10.1016/j.jad.2012.07.019 · Cited by 87 · see citing works
Siller, S. S., & Broadie, K. S. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.008045 · Cited by 86 · see citing works
Persistent decrease in multiple components of the perineuronal net following status epilepticus
McRae, P. A., Baranov, E., Rogers, S. L., & Porter, B. E. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08268.x · Cited by 85 · 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
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
Impaired Critical Period Plasticity in Primary Auditory Cortex of Fragile X Model Mice
Kim, H., Gibboni, R., Kirkhart, C., & Bao, S. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3246-12.2013 · Cited by 74 · cited 4× · see citing works
“Though other MMPs are increased as well, including MMP-2, MMP-3 and TIMP-2 in adults, MMP-9 has the most prominent and consistent increase in protein levels across ages (Konopka et al., 2013).”
BackgroundInfluentialSuenaga, N., Ichiyama, T., Kubota, M., Isumi, H., Tohyama, J., & Furukawa, S. (2007) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.09.011 · Cited by 73 · see citing works
Shubayev, V. I., & Myers, R. R. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20160 · Cited by 71 · see citing works
Amniotic Fluid MMP ‐9 and Neurotrophins in Autism Spectrum Disorders: An Exploratory Study
Abdallah, M. W., Pearce, B. D., Larsen, N., Greaves‐Lord, K., Nørgaard‐Pedersen, B., HOUGAARD, D. M., Mortensen, E. L., & Grove, J. (2012) · Autism Research · doi:10.1002/aur.1254 · Cited by 69 · see citing works
Matrix Metalloproteinases and Minocycline: Therapeutic Avenues for Fragile X Syndrome
Siller, S. S., & Broadie, K. S. (2012) · Neural Plasticity · doi:10.1155/2012/124548 · Cited by 68 · see citing works
Matrix metalloproteinase-9 (MMP-9) in human intractable epilepsy caused by focal cortical dysplasia
Konopka, A., Grajkowska, W., Ziemiańska, K., Roszkowski, M., Daszkiewicz, P., Rysz, A., Marchel, A., Koperski, Ł., Wilczynski, G. M., & Dzwonek, J. (2012) · Epilepsy Research · doi:10.1016/j.eplepsyres.2012.09.018 · Cited by 68 · see citing works
Szepesi, Z., Bijata, M., Ruszczycki, B., Kaczmarek, L., & Włodarczyk, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063314 · Cited by 68 · see citing works
Interactions between ICAM-5 and β1 integrins regulate neuronal synapse formation
Ning, L., Tian, L., Smirnov, S., Vihinen, H., Llano, O., Vick, K. A., Davis, R. L., Rivera, C., & Gahmberg, C. G. (2012) · Journal of Cell Science · doi:10.1242/jcs.106674 · Cited by 67 · see citing works
Casting a net on dendritic spines: The extracellular matrix and its receptors
Dansie, L. E., & Ethell, I. M. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20963 · Cited by 66 · see citing works
Self-citationLatent MMP-9 is bound to TIMP-1 before secretion
Roderfeld, M., Graf, J., Giese, B., Salguero-Palacios, R., Tschuschner, A., Müller‐Newen, G., & Roeb, E. (2007) · Biological Chemistry · doi:10.1515/bc.2007.123 · Cited by 66 · see citing works
Ye, P., Carson, J. L., & D’Ercole, A. J. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)12194-3 · Cited by 65 · see citing works
A critical period during postnatal auditory development of mice
Webster, D. B. (1984) · International Journal of Pediatric Otorhinolaryngology · doi:10.1016/s0165-5876(83)80111-6 · Cited by 63 · see citing works
Hehr, C. L., Hocking, J. C., & McFarlane, S. (2005) · Development · doi:10.1242/dev.01908 · Cited by 62 · see citing works
The effect of minocycline on seizures induced by amygdala kindling in rats
Nasr, S. M. B., Moghimi, A., Mohammad‐Zadeh, M., Shamsizadeh, A., & Noorbakhsh, S. M. (2013) · Seizure · doi:10.1016/j.seizure.2013.05.005 · Cited by 62 · 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
Kaliszewska, A., Bijata, M., Kaczmarek, L., & Kossut, M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr303 · Cited by 55 · see citing works
Looking forward to EphB signaling in synapses
Sloniowski, S., & Ethell, I. M. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.10.020 · Cited by 54 · see citing works
Self-citationBuilding and remodeling synapses
Benson, D. L., & Huntley, G. W. (2010) · Hippocampus · doi:10.1002/hipo.20872 · Cited by 48 · see citing works
Fibronectin attenuates process outgrowth in oligodendrocytes by mislocalizing MMP-9 activity
Šišková, Z., Yong, V. W., Nomden, A., van Strien, M. E., Hoekstra, D., & Baron, W. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.07.005 · Cited by 48 · see citing works
The role of matrix metalloproteinases in the morphogenesis of the cerebellar cortex
Luo, J. (2005) · The Cerebellum · doi:10.1080/14734220500247646 · Cited by 46 · see citing works
Aujla, P. K., & Huntley, G. W. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23468 · Cited by 39 · see citing works
Serfaty, C. A., Campello‐Costa, P., & Linden, R. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.04.005 · Cited by 38 · 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
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 · see citing works
Matrix Metalloproteinase-9 Regulates Survival of Neurons in Newborn Hippocampus
Murase, S., & McKay, R. D. G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.297671 · Cited by 34 · see citing works
Minocycline increases phosphorylation and membrane insertion of neuronal GluR1 receptors
Imbesi, M., Uz, T., Manev, R., Sharma, R. P., & Manev, H. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.10.006 · Cited by 34 · see citing works
Oliveira-Silva, P., Jurgilas, P. B., Trindade, P., Campello‐Costa, P., Perales, J., Savino, W., & Serfaty, C. A. (2007) · NeuroImmunoModulation · doi:10.1159/000110638 · Cited by 34 · see citing works
Distinct patterns of matrix metalloproteinase-2 and -9 expression in normal human cell lines
Niedzwiecki (2009) · Oncology Reports · doi:10.3892/or_00000290 · Cited by 34 · see citing works
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 32 · see citing works
Maier, O., van der Heide, T., Johnson, R. S., de Vries, H., Baron, W., & Hoekstra, D. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.11.014 · Cited by 29 · 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
The Barrel Cortex as a Model to Study Dynamic Neuroglial Interaction
Giaume, C., Maravall, M., Welker, E., & Bonvento, G. (2009) · The Neuroscientist · doi:10.1177/1073858409336092 · Cited by 28 · see citing works
Kelly, 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 · see citing works
Response of matrix metalloproteinase-9 to olfactory nerve injury
Costanzo, R. M., Perrino, L. A., & Kobayashi, M. (2006) · Neuroreport · doi:10.1097/wnr.0b013e32800fef87 · Cited by 20 · see citing works
Development of the Nervous System
Pomeroy, S. L., & Ullrich, N. J. (2004) · Elsevier eBooks · doi:10.1016/b978-0-7216-9654-6.50168-5 · Cited by 11 · see citing works
Imaging the plasticity of the central auditory system on the cellular and molecular level
Illing, R., Roßkothen-Kuhl, N., Fredrich, M., Hildebrandt, H., & Zeber, A. C. (2009) · Hearing Balance and Communication · doi:10.3109/16513860903454583 · Cited by 10 · see citing works
Piccolini, V. M., Avella, D., Bottone, M. G., Bottiroli, G. F., & Bernocchi, G. (2012) · Brain Research · doi:10.1016/j.brainres.2012.09.025 · Cited by 9 · see citing works
Inhibition of MMP-2 but not MMP-9 Influences Inner Ear Spiral Ganglion Neurons In Vitro
Sung, M. L., Wei, E., Chávez, E., Jain, N., Levano, S., Binkert, L., Ramseier, A., Setz, C., Bodmer, D., Ryan, A. F., et al. (2014) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-014-0077-2 · Cited by 8 · see citing works
Kelly, E. A., Tremblay, M., Gahmberg, C. G., Tian, L., & Majewska, A. K. (2013) · Communicative & Integrative Biology · doi:10.4161/cib.27315 · Cited by 5 · see citing works
Pizer, I. H. (1990) · PubMed · Cited by 4 · see citing works
Structural Organization of the Barrel Cortex in Rats (an immunohistochemical study)
Logvinov, A. K., Kirichenko, E. Y., Повилайтите, П. Е., & Сухов, А. Г. (2010) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-010-9387-0 · Cited by 4 · see citing works
Flagged first, then by citations
1 of the 145 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Matrix Metalloproteinase-9 (MMP-9) as a Cancer Biomarker and MMP-9 Biosensors: Recent Advances
Huang, H. (2018) · Sensors · doi:10.3390/s18103249 · Cited by 741 · see citing works
Resveratrol regulates neuro-inflammation and induces adaptive immunity in Alzheimer’s disease
Moussa, C., Hebron, M. L., Huang, X., Ahn, J., Rissman, R. A., Aisen, P. S. S., & Turner, R. S. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0779-0 · Cited by 712 · see citing works
Neuronal regulation of the blood–brain barrier and neurovascular coupling
Kaplan, L., Chow, B. W., & Gu, C. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0322-2 · Cited by 431 · see citing works
MMP ‐9 in translation: from molecule to brain physiology, pathology, and therapy
Vafadari, B., Salamian, A., & Kaczmarek, L. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13415 · Cited by 381 · see citing works
Perineuronal Nets: Plasticity, Protection, and Therapeutic Potential
Reichelt, A. C., Hare, D. J., Bussey, T. J., & Saksida, L. M. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.04.003 · Cited by 219 · see citing works
Plasticity of Spine Structure: Local Signaling, Translation and Cytoskeletal Reorganization
Nakahata, Y., & Yasuda, R. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00029 · Cited by 209 · 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
Oxidative Stress-Mediated Blood-Brain Barrier (BBB) Disruption in Neurological Diseases
Song, K., Li, Y., Zhang, H., An, N., Wei, Y., Wang, L., Tian, C., Yuan, M., Sun, Y., Xing, Y., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/4356386 · Cited by 199 · see citing works
The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders
Wen, T. H., Binder, D. K., Ethell, I. M., & Razak, K. A. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00270 · Cited by 170 · see citing works
Self-citationWen, 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
Self-citationShaping 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
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 · see citing works
Greiss Hess, L., Fitzpatrick, S. E., Nguyen, D. V., Chen, Y., Gaul, K. N., Schneider, A., Lemons Chitwood, K., Eldeeb, M. A. A. A., Polussa, J., Hessl, D., et al. (2016) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0000000000000334 · Cited by 122 · see citing works
Lovelace, J. W., Wen, T. H., Reinhard, S., Hsu, M. S., Sidhu, H., Ethell, I. M., Binder, D. K., & Razak, K. A. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.02.002 · Cited by 115 · see citing works
Self-citationNovel Matrix Metalloproteinase-9 (MMP-9) Inhibitors in Cancer Treatment
Rashid, Z. A., & Bardaweel, S. K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512133 · Cited by 119 · see citing works
Banerjee, A., Ifrim, M. F., Valdez‐Sinon, A. N., Raj, N., & Bassell, G. J. (2018) · Brain Research · doi:10.1016/j.brainres.2018.04.008 · Cited by 103 · see citing works
The Degradome database: expanding roles of mammalian proteases in life and disease
Pérez-Silva, J. G., Español, Y., Velasco, G., & Quesada, V. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1201 · Cited by 97 · see citing works
Gene expression profiling reveals a conserved microglia signature in larval zebrafish
Mazzolini, J., Clerc, S. L., Morisse, G., Coulonges, C., Kuil, L. E., van Ham, T. J., Zagury, J., & Sieger, D. (2019) · Glia · doi:10.1002/glia.23717 · Cited by 90 · see citing works
Vahsen, B. F., Nalluru, S., Morgan, G. R., Farrimond, L. E., Carroll, E., Xu, Y., Cramb, K. M. L., Amein, B., Scaber, J., Katsikoudi, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41603-0 · Cited by 78 · see citing works
Perineuronal net degradation rescues CA2 plasticity in a mouse model of Rett syndrome
Carstens, K. E., Lustberg, D. J., Shaughnessy, E. K., McCann, K. E., Alexander, G. M., & Dudek, S. M. (2021) · Journal of Clinical Investigation · doi:10.1172/jci137221 · Cited by 57 · see citing works
Campanari, M.-L., García-Ayllón, M.-S., Ciura, S., Sáez-Valero, J., & Kabashi, E. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00160 · Cited by 69 · see citing works
Role of MMP-9 in epithelial-mesenchymal transition of thyroid cancer
Li, Y., He, J., Wang, F., Wang, X., Yang, F., Zhao, C., Feng, C., & Li, T. (2020) · World Journal of Surgical Oncology · doi:10.1186/s12957-020-01958-w · Cited by 67 · see citing works
MMPs and ADAMs in neurological infectious diseases and multiple sclerosis
Muri, L., Leppert, D., Grandgirard, D., & Leib, S. L. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03174-6 · Cited by 64 · see citing works
Research progress of mechanisms for tight junction damage on blood–brain barrier inflammation
Zhao, B., Yin, Q., Fei, Y., Zhu, J., Qiu, Y.-Y., Fang, W., & Li, Y. (2020) · Archives of Physiology and Biochemistry · doi:10.1080/13813455.2020.1784952 · Cited by 65 · see citing works
Koskinen, M.-K., van Mourik, Y., Smit, A. B., Riga, D., & Spijker, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-73173-2 · Cited by 61 · see citing works
Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice
Brewton, D. H., Kokash, J., Jimenez, O., Pena, E. R., & Razak, K. A. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00270 · Cited by 54 · see citing works
Self-citationBlast-induced temporal alterations in blood–brain barrier properties in a rodent model
Kawoos, U., Abutarboush, R., Gu, M., Chen, Y., Statz, J. K., Goodrich, S. Y., & Ahlers, S. T. (2021) · Scientific Reports · doi:10.1038/s41598-021-84730-8 · Cited by 58 · see citing works
Incubation of depression: ECM assembly and parvalbumin interneurons after stress
Spijker, S., Koskinen, M.-K., & Riga, D. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.07.015 · Cited by 55 · see citing works
Long, K. R., & Huttner, W. Β. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.804649 · Cited by 57 · see citing works
Matrix metalloproteinases in the CNS: interferons get nervous
Chopra, S., Overall, C. M., & Dufour, A. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03171-9 · Cited by 55 · see citing works
Jorgačevski, J., Zorec, R., & Potokar, M. (2020) · Cells · doi:10.3390/cells9122622 · Cited by 54 · see citing works
Do, P. T., Wu, C.-C., Chiang, Y. H., Hu, C., & Chen, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221810045 · Cited by 53 · see citing works
Ahluwalia, M., Kumar, M., Ahluwalia, P. K., Rahimi, S. Y., Vender, J. R., Raju, R. P., Hess, D. C., Baban, B., Vale, F. Ĺ., Dhandapani, K. M., et al. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.105192 · Cited by 54 · see citing works
Matrix Metalloproteinase-9 as an Important Contributor to the Pathophysiology of Depression
Li, H., Sheng, Z., Khan, S., Zhang, R., Liu, Y., Zhang, Y., Yong, V. W., & Xue, M. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.861843 · Cited by 54 · see citing works
Neural Correlates of Auditory Hypersensitivity in Fragile X Syndrome
Razak, K., Binder, D., & Ethell, I. M. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.720752 · Cited by 47 · see citing works
Self-citationAutism‐related behaviors in the cyclooxygenase‐2‐deficient mouse model
Wong, C. T., Bestard‐Lorigados, I., & Crawford, D. A. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12506 · Cited by 51 · see citing works
Sevenoaks, T., Wedderburn, C. J., Donald, K. A., Barnett, W., Zar, H. J., Stein, D. J., & Naudé, P. J. W. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.08.021 · Cited by 50 · see citing works
Two matrix metalloproteinase classes reciprocally regulate synaptogenesis
Dear, M. L., Dani, N., Parkinson, W. M., Zhou, S., & Broadie, K. S. (2015) · Development · doi:10.1242/dev.124461 · Cited by 49 · see citing works
Shabani, E., Abdekhodaie, M. J., Mousavi, S. A., & Taghipour, F. (2020) · Biochemical Engineering Journal · doi:10.1016/j.bej.2020.107772 · Cited by 47 · see citing works
A randomized controlled trial of sertraline in young children with autism spectrum disorder
Potter, L. A., Scholze, D. A., Biag, H. M. B., Schneider, A., Chen, Y., Nguyen, D. V., Rajaratnam, A., Rivera, S. M., Dwyer, P. S., Tassone, F., et al. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00810 · Cited by 43 · see citing works
Nadanaka, S., Miyata, S., Yaqiang, B., Tamura, J.-I., Habuchi, O., & Kitagawa, H. (2020) · Biomolecules · doi:10.3390/biom10111499 · Cited by 43 · 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
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 40 · see citing works
Mani, S., Dubey, R., Lai, I., Babu, M. A., Tyagi, S., Swargiary, G., Mody, D., Singh, M., Agarwal, S., Iqbal, D., et al. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-220700 · Cited by 40 · see citing works
Reichelt, A. C., Lemieux, C. A., Princz‐Lebel, O., Singh, A., Bussey, T. J., & Saksida, L. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-85092-x · Cited by 39 · see citing works
Cheung, S. W., Bhavnani, E., Simmons, D. G., Bellingham, M. C., & Noakes, P. G. (2024) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12982 · Cited by 35 · see citing works
Minocycline Treatment Reverses Sound Evoked EEG Abnormalities in a Mouse Model of Fragile X Syndrome
Lovelace, J. W., Ethell, I. M., Binder, D. K., & Razak, K. A. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00771 · Cited by 36 · see citing works
Self-citationNon-Cell-Autonomous Factors Implicated in Parvalbumin Interneuron Maturation and Critical Periods
Gibel-Russo, R., Benacom, D., & Nardo, A. A. D. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.875873 · Cited by 36 · see citing works
Le, N. D., Muri, L., Grandgirard, D., Kühle, J., Leppert, D., & Leib, S. L. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01966-3 · Cited by 35 · see citing works
Wang, J., & Zhang, Y. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8674 · Cited by 35 · see citing works
Neuro-Axonal Damage and Alteration of Blood–Brain Barrier Integrity in COVID-19 Patients
Zingaropoli, M. A., Iannetta, M., Piermatteo, L., Pasculli, P., Latronico, T., Mazzuti, L., Campogiani, L., Duca, L., Ferraguti, G., Michele, M. D., et al. (2022) · Cells · doi:10.3390/cells11162480 · Cited by 34 · see citing works
Molecular Biomarkers in Fragile X Syndrome
Zafarullah, M., & Tassone, F. (2019) · Brain Sciences · doi:10.3390/brainsci9050096 · Cited by 36 · 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
Deckmann, I., Santos‐Terra, J., Fontes‐Dutra, M., Rockenbach, M. K., Bauer‐Negrini, G., Schwingel, G. B., Riesgo, R. D. S., Bambini-Júnior, V., & Gottfried, C. (2021) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10137 · Cited by 34 · see citing works
Reinhard, S. M., Rais, M., Afroz, S., Hanania, Y., Pendi, K., Espinoza, K., Rosenthal, R., Binder, D. K., Ethell, I. M., & Razak, K. A. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107042 · Cited by 33 · see citing works
Self-citationBiswas, M. H. U., Almeida, S., Lopez-Gonzalez, R., Mao, W., Zhang, Z., Karydas, A., Geschwind, M. D., Biernat, J., Mandelkow, E., Futai, K., et al. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.08.006 · Cited by 33 · see citing works
Therapeutic Effects of a Novel Form of Biotin on Propionic Acid-Induced Autistic Features in Rats
Şahin, K., Orhan, C., Karatoprak, S., Tuzcu, M., Deeh, P. B. D., Özercan, İ. H., Şahin, N., Bozoğlan, M. Y., Sylla, S., Ojalvo, S. P., et al. (2022) · Nutrients · doi:10.3390/nu14061280 · Cited by 32 · see citing works
Pasquet, N., Douceau, S., Naveau, M., Lesept, F., Louessard, M., Lebouvier, L., Hommet, Y., Vivien, D., & Bardou, I. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy119 · Cited by 31 · see citing works
Toledo, M. A., Wen, T. H., Binder, D. K., Ethell, I. M., & Razak, K. A. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112068 · Cited by 31 · see citing works
Self-citationMMP-9 Contributes to Dendritic Spine Remodeling Following Traumatic Brain Injury
Pijet, B., Stefaniuk, M., & Kaczmarek, L. (2019) · Neural Plasticity · doi:10.1155/2019/3259295 · Cited by 31 · see citing works
Tissue inhibitors of metalloproteinases are proteolytic targets of matrix metalloproteinase 9
Coates-Park, S., Lazaroff, C., Gurung, S., Rich, J. A., Colladay, A., O’Neill, M. J., Butler, G. S., Overall, C. M., Stetler‐Stevenson, W. G., & Peeney, D. (2023) · Matrix Biology · doi:10.1016/j.matbio.2023.09.002 · Cited by 30 · see citing works
Dear, M. L., Shilts, J., & Broadie, K. (2017) · Science Signaling · doi:10.1126/scisignal.aan3181 · Cited by 29 · see citing works
Kokash, J., Alderson, E. M., Reinhard, S. M., Crawford, C. A., Binder, D. K., Ethell, I. M., & Razak, K. A. (2019) · Brain Research · doi:10.1016/j.brainres.2019.05.029 · Cited by 29 · see citing works
Self-citationOvsepian, S. V., O’Leary, V. B., & Martı́nez, S. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02728-6 · Cited by 29 · see citing works
Impact of maternal immune activation on dendritic spine development
Pękała, M., Doliwa, M., & Kalita, K. B. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22804 · Cited by 26 · see citing works
Sanapalli, B. K. R., Yele, V., Jupudi, S., & Karri, V. V. S. R. (2021) · RSC Advances · doi:10.1039/d1ra03891e · Cited by 28 · see citing works
Akol, I., Kalogeraki, E., Pielecka-Fortuna, J., Fricke, M., & Löwel, S. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0902-21.2021 · Cited by 28 · see citing works
GPR18 drives FAAH inhibition-induced neuroprotection against HIV-1 Tat-induced neurodegeneration
Hermes, D. J., Yadav-Samudrala, B. J., Xu, C., Paniccia, J. E., Meeker, R. B., Armstrong, M., Reisdorph, N. A., Cravatt, B. F., Mackie, K., Lichtman, A. H., et al. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113699 · Cited by 27 · see citing works
In Vivo Volume Dynamics of Dendritic Spines in the Neocortex of Wild-Type and Fmr1 KO Mice
Ishii, K., Nagaoka, A., Kishida, Y., Okazaki, H., Yagishita, S., Ucar, H., Takahashi, N. K., Saito, N., & Kasai, H. (2018) · eNeuro · doi:10.1523/eneuro.0282-18.2018 · Cited by 25 · see citing works
Lysophosphatidic Acid Signalling in Nervous System Development and Function
Birgbauer, E. (2020) · NeuroMolecular Medicine · doi:10.1007/s12017-020-08630-2 · Cited by 27 · see citing works
Sullivan, G., Galdi, P., Borbye‐Lorenzen, N., Stoye, D. Q., Lamb, G. J., Evans, M. J., Skogstrand, K., Chandran, S., & Boardman, J. P. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.722489 · Cited by 26 · see citing works
Dumbuya, J. S., Chen, X., Du, J., Li, S., Liang, L., Xie, H., & Zeng, Q. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110758 · Cited by 26 · 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
Computational study of effective matrix metalloproteinase 9 (MMP9) targeting natural inhibitors
Liu, N., Wang, X., Wu, H., Lv, X., Xie, H., Guo, Z., Wang, J., Dou, G., Zhang, C., & Sun, M. (2021) · Aging · doi:10.18632/aging.203581 · Cited by 25 · see citing works
Ibi, D., & Yamada, K. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226092 · Cited by 24 · 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
Dolutegravir Inhibition of Matrix Metalloproteinases Affects Mouse Neurodevelopment
Bade, A. N., McMillan, J., Liu, Y., Edagwa, B., & Gendelman, H. E. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02508-5 · Cited by 28 · see citing works
Wang, J., Ren, D.-P., Sun, Y., Xu, C., Wang, C., Cheng, R., Wang, L., Jia, G., Ren, J., Ma, J., et al. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14996 · 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
Arkadash, V., Radisky, E. S., & Papo, N. (2018) · Oncotarget · doi:10.18632/oncotarget.25885 · 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
Altered extracellular matrix structure and elevated stiffness in a brain organoid model for disease
Zur, M. K., Bhattacharya, B., Solomonov, I., Dror, S. B., Savidor, A., Levin, Y., Prior, A., Sapir, T., Harris, T., Olender, T., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59252-w · Cited by 23 · see citing works
MMP-9 Signaling Pathways That Engage Rho GTPases in Brain Plasticity
Figiel, I., Kruk, P. K., Zaręba-Kozioł, M., Rybak, P., Bijata, M., Włodarczyk, J., & Dzwonek, J. (2021) · Cells · doi:10.3390/cells10010166 · Cited by 22 · see citing works
Neuroglia Cells Transcriptomic in Brain Development, Aging and Neurodegenerative Diseases
Pinosanu, L. R., Căpitănescu, B., Glăvan, D., Godeanu, S., Fernández‐Cadenas, I., Doeppner, T. R., Hermann, D. M., Bălşeanu, T. A., Cătălin, B., & Popa‐Wagner, A. (2022) · Aging and Disease · doi:10.14336/ad.2022.0621 · Cited by 22 · see citing works
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 22 · see citing works
NG2 Glia: Novel Roles beyond Re-/Myelination
Parolisi, R., & Boda, E. (2018) · Neuroglia · doi:10.3390/neuroglia1010011 · Cited by 21 · see citing works
An “Omic” Overview of Fragile X Syndrome
Dionne, O., & Corbin, F. (2021) · Biology · doi:10.3390/biology10050433 · Cited by 22 · see citing works
Agoston, D. V., McCullough, J., Aniceto, R., Lin, I.-H., Kamnaksh, A., Eklund, M., Graves, W. M., Dunbar, C., Engall, J., Schneider, E. B., et al. (2022) · Neurotrauma Reports · doi:10.1089/neur.2022.0029 · Cited by 21 · see citing works
Трофимов, А. Н., Strekalova, T. V., Mortimer, N., Zubareva, O. E., Schwarz, A. P., Svirin, E. P., Umriukhin, A., Svistunov, A. A., Lesch, K., & Клименко, В. М. (2017) · Neurotoxicity Research · doi:10.1007/s12640-017-9720-2 · Cited by 21 · see citing works
HIV-1 Integrase Strand Transfer Inhibitors and Neurodevelopment
Foster, E. G., Gendelman, H. E., & Bade, A. N. (2022) · Pharmaceuticals · doi:10.3390/ph15121533 · Cited by 20 · see citing works
Metalloproteinases as Biomarkers and Sociomarkers in Human Health and Disease
Costa, D., Scalise, E., Ielapi, N., Bracale, U. M., Andreucci, M., & Serra, R. (2024) · Biomolecules · doi:10.3390/biom14010096 · Cited by 22 · see citing works
Islam, Y., Khalid, A., Pluchino, S., Sivakumaran, M., Teixidò, M., Leach, A. G., Fatokun, A. A., Downing, J., Coxon, C. R., & Ehtezazi, T. (2020) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2020.06.021 · Cited by 19 · see citing works
Çiçek, A. U., Işık, C. M., Bakır, S., Özbek, D. Ü., Sarı, S. A., Bakır, D., & Cam, S. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02231-w · Cited by 19 · see citing works
Bobotis, B. C., Halvorson, T., Carrier, M., & Tremblay, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1317125 · Cited by 21 · 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
Hodges, S. L., Nolan, S. O., Tomac, L. A., Muhammad, I. D. A., Binder, M. S., Taube, J. H., & Lugo, J. N. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112776 · Cited by 19 · see citing works
MicroRNAs: Possible Regulatory Molecular Switch Controlling the BBB Microenvironment
Chakraborty, C., Sharma, A. R., Sharma, G., Bhattacharya, M., & Lee, S. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.12.024 · Cited by 18 · see citing works
Porter, K. N., Sarkar, S. N., Dakhlallah, D. A., Vannoy, M. E., Quintana, D. D., & Simpkins, J. W. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00092 · Cited by 17 · see citing works
Włodarczyk, L., Cichoń, N., Karbownik, M. S., Saso, L., Saluk, J., & Miller, E. D. (2023) · Brain Sciences · doi:10.3390/brainsci13060846 · Cited by 17 · see citing works
Inhibition of MMP-9 attenuates hypertensive cerebrovascular dysfunction in Dahl salt-sensitive rats
Kalani, A., Pushpakumar, S. B., Vacek, J. C., Tyagi, S. C., & Tyagi, N. (2016) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2623-8 · Cited by 17 · see citing works
- Authors
- Reinhard, S. M., Razak, K., & Ethell, I. M.
- Affiliations
- University of California, Riverside (US)
- Corresponding author
- Ethell, Iryna M.
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2015-07-29
- Volume
- 9
- Pages
- 280-280
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC4518323
- OpenAlex
- W1504544942
- Cited by
- 219
- References
- 145
- Citations by year
- 2026: 9 · 2025: 18 · 2024: 16 · 2023: 28 · 2022: 32 · 2021: 34 · 2020: 29 · 2019: 17 · 2018: 14 · 2017: 7 · 2016: 11 · 2015: 4
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Science Foundation
- FRAXA Research Foundation
- National Institute of Mental Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- MMP-9, extracellular matrix, brain development, neurodevelopmental disorders, critical period, synaptogenesis, axon guidance, myelination, synaptic plasticity, fragile X syndrome, traumatic brain injury, multiple sclerosis, Alzheimer's disease
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
