A normal genetic variation modulates synaptic MMP-9 protein levels and the severity of schizophrenia symptoms.
Open accessAbstract
Matrix metalloproteinase 9 (MMP-9) has recently emerged as a molecule that contributes to pathological synaptic plasticity in schizophrenia, but explanation of the underlying mechanisms has been missing.In the present study, we performed a phenotypebased genetic association study (PGAS) in > 1,000 schizophrenia patients from the Göttingen Research Association for Schizophrenia (GRAS) data collection and found an association between the MMP-9 rs20544 C/T single-nucleotide polymorphism (SNP) located in the 3 0 untranslated region (UTR) and the severity of a chronic delusional syndrome.In cultured neurons, the rs20544 SNP influenced synaptic MMP-9 activity and the morphology of dendritic spines.We demonstrated that Fragile X mental retardation protein (FMRP) bound the MMP-9 3 0 UTR.We also found dramatic changes in RNA structure folding and alterations in the affinity of FMRP for MMP-9 RNA, depending on the SNP variant.Finally, we observed greater sensitivity to psychosis-related locomotor hyperactivity in Mmp-9 heterozygous mice.We propose a novel mechanism that involves MMP-9-dependent changes in dendritic spine morphology and the pathophysiology of schizophrenia, providing the first mechanistic insights into the way in which the single base change in the MMP-9 gene (rs20544) influences gene function and results in phenotypic changes observed in schizophrenia patients.
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A functional polymorphism of the MMP-9 gene was discovered in human schizophrenia patients.
“A functional polymorphism of the MMP-9 gene was discovered in human schizophrenia patients (Rybakowski et al., 2009; Lepeta et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Lepeta et al., 2017
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Cites
Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
The Positive and Negative Syndrome Scale (PANSS) for schizophrenia.
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987) · Schizophrenia Bulletin · doi:10.1093/schbul/13.2.261 · Cited by 21,378 · see citing works
Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision (DSM-IV-TR)
American Psychiatric Association (2000) · doi:10.1176/appi.books.9780890423349 · Cited by 11,069 · see citing works
(1976) · Medical Entomology and Zoology · Cited by 8,899 · see citing works
Biological insights from 108 schizophrenia-associated genetic loci
Schizophrenia Working Group of the Psychiatric Genomics Consortium (2014) · Nature · doi:10.1038/nature13595 · Cited by 7,577 · see citing works
Self-citationA pyramid approach to subpixel registration based on intensity
Thévenaz, P., Ruttimann, U. E., & Unser, M. A. (1998) · IEEE Transactions on Image Processing · doi:10.1109/83.650848 · Cited by 3,097 · see citing works
FMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism
Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y. S., Mele, A., Fraser, C. E., Stone, E. F., Chen, C., Fak, J. J., Chi, S. W., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.013 · Cited by 2,072 · see citing works
Dendritic spine pathology in neuropsychiatric disorders
Penzes, P., Cahill, M. E., Jones, K. A., VanLeeuwen, J.-E., & Woolfrey, K. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2741 · Cited by 1,523 · see citing works
Harris, K., & Stevens, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02982.1989 · Cited by 1,073 · see citing works
mRNA localization: Gene expression in the spatial dimension
Martin, K. C., & Ephrussi, A. (2009) · Cell · doi:10.1016/j.cell.2009.01.044 · Cited by 1,048 · see citing works
Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits
Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., & Greenough, W. T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5401 · Cited by 1,046 · see citing works
QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences
Kikin, O., D'Antonio, L., & Bagga, P. (2006) · Nucleic Acids Res. · doi:10.1093/nar/gkl253 · Cited by 974 · see citing works
Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function
Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T., & Darnell, R. B. (2001) · Cell · doi:10.1016/s0092-8674(01)00566-9 · Cited by 952 · see citing works
Automated 3D structure composition for large RNAs
Popenda, M., Szachniuk, M., Antczak, M., Purzycka, K. J., Łukasiak, P., Bartol, N., Błażewicz, J., & Adamiak, R. W. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks339 · Cited by 761 · see citing works
Self-citationPsychiatric genome-wide association study analyses implicate neuronal, immune and histone pathways
The Network and Pathway Analysis Subgroup of the Psychiatric Genomics Consortium (2015) · Nature Neuroscience · doi:10.1038/nn.3922 · Cited by 755 · see citing works
Accurate SHAPE-directed RNA structure determination
Deigan, K. E., Li, T. W., Mathews, D. H., & Weeks, K. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806929106 · Cited by 697 · see citing works
Zalfa, F., Giorgi, M., Primerano, B., Moro, A., Di Penta, A., Reis, S., Oostra, B., & Bagni, C. (2003) · Cell · doi:10.1016/s0092-8674(03)00079-5 · Cited by 676 · see citing works
Genesis of dendritic spines: insights from ultrastructural and imaging studies
Yuste, R., & Bonhoeffer, T. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1300 · Cited by 628 · see citing works
Dendritic spine pathology in schizophrenia
Glausier, J. R., & Lewis, D. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.044 · Cited by 581 · see citing works
Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies
Arellano, J. I. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.010.2007 · Cited by 529 · see citing works
Hou, L., Antion, M. D., Hu, D., Spencer, C. M., Paylor, R., & Klann, E. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.005 · Cited by 469 · 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
Muddashetty, R. S., Kelić, S., Gross, C., Xu, M., & Bassell, G. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0937-07.2007 · Cited by 421 · see citing works
Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R. D. G., & Kaczmarek, L. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00920.2002 · Cited by 392 · see citing works
Self-citationMMP ‐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
Self-citationGurling, H., Kalsi, G., Brynjolfsson, J., Sigmundsson, T., Sherrington, R. P., Mankoo, B. S., Read, T., Murphy, P. L., Blaveri, E., McQuillin, A., et al. (2001) · The American Journal of Human Genetics · doi:10.1086/318788 · Cited by 373 · see citing works
Adult fragile X syndrome: Clinico-neuropathologic findings
Rudelli, R. D., Brown, W. T., Wisniewski, K., Jenkins, E. C., Laure-Kamionowska, M., Connell, F., & Wisniewski, H. M. (1985) · Acta Neuropathologica · doi:10.1007/bf00687814 · Cited by 362 · 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
Hammer, C., Stepniak, B., Schneider, A., Papiol, S., Tantra, M., Begemann, M., Sirén, A.-L., Pardo, L. A., Sperling, S., Mohd Jofrry, S., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.110 · Cited by 342 · see citing works
Self-citationvan den Buuse, M. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp132 · Cited by 340 · 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
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
Self-citationSynaptic circuit remodelling by matrix metalloproteinases in health and disease
Huntley, G. W. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3320 · Cited by 282 · see citing works
Forskolin-Induced LTP in the CA1 Hippocampal Region Is NMDA Receptor Dependent
Otmakhov, N., Khibnik, L. A., Otmakhova, N. A., Carpenter, S. M., Riahi, S., Asrican, B., & Lisman, J. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00941.2003 · Cited by 254 · see citing works
Lin, Y., & Koleske, A. J. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153204 · Cited by 241 · see citing works
Vasa, S. M., Guex, N., Wilkinson, K. A., Weeks, K. M., & Giddings, M. C. (2008) · RNA · doi:10.1261/rna.1166808 · Cited by 229 · see citing works
The positive and negative syndrome scale for schizophrenia
Obermeier, M. (2012) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.14936 · Cited by 226 · 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
The acute effects of NMDA antagonism: from the rodent to the human brain.
Gunduz-Bruce, H. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.07.006 · Cited by 182 · 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
Self-citationSidhu, 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
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
Self-citationStepniak, B., Papiol, S., Hammer, C., Ramin, A., EVERTS, S., Hennig, L., Begemann, M., & Ehrenreich, H. (2014) · The Lancet Psychiatry · doi:10.1016/s2215-0366(14)70379-7 · Cited by 120 · see citing works
Self-citationThe 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
Self-citationYamamori, 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
The formation pathway of tetramolecular G-quadruplexes
Bardin, C., & Leroy, J. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1050 · Cited by 97 · see citing works
Extracellular matrix control of dendritic spine and synapse structure and plasticity in adulthood
Levy, A. D., Omar, M. H., & Koleske, A. J. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00116 · Cited by 96 · see citing works
Modification of Cognitive Performance in Schizophrenia by Complexin 2 Gene Polymorphisms
Begemann, M., Grube, S., Papiol, S., Malzahn, D., Krampe, H., Ribbe, K., Friedrichs, H., Radyushkin, K., El-Kordi, A., Benseler, F., et al. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.107 · Cited by 94 · see citing works
Self-citationRNAComposer and RNA 3D structure prediction for nanotechnology
Biesiada, M., Pachulska‐Wieczorek, K., Adamiak, R. W., & Purzycka, K. J. (2016) · Methods · doi:10.1016/j.ymeth.2016.03.010 · Cited by 88 · see citing works
Self-citationmiR-132 Regulates Dendritic Spine Structure by Direct Targeting of Matrix Metalloproteinase 9 mRNA
Jasińska, M., Miłek, J., Cymerman, I. A., Łęski, S., Kaczmarek, L., & Dziembowska, M. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9383-z · Cited by 83 · see citing works
Self-citationSzepesi, 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
Self-citationRNA ‐binding proteins, neural development and the addictions
Bryant, C. D., & Yazdani, N. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12273 · Cited by 79 · see citing works
Functional polymorphism of the matrix metalloproteinase-9 (MMP-9) gene in schizophrenia.
Rybakowski, J. K., Skibinska, M., Kapelski, P., Kaczmarek, L., & Hauser, J. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.02.005 · Cited by 76 · see citing works
Self-citationSampling issues in quantitative analysis of dendritic spines morphology
Ruszczycki, B., Szepesi, Z., Wilczynski, G. M., Bijata, M., Kalita, K. B., Kaczmarek, L., & Włodarczyk, J. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-213 · Cited by 75 · see citing works
Self-citationMatrix 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
Self-citationJean, P. L. S., ZHANG, X. C., Hart, B. K., Lamlum, H., Webster, M. W., Steed, D. L., HENNEY, A. M., & Ferrell, R. E. (1995) · Annals of Human Genetics · doi:10.1111/j.1469-1809.1995.tb01602.x · Cited by 74 · see citing works
Chang, S.-H., Chiang, S., Chiu, C., Tsai, C.-C., Tsai, H.-H., Huang, C., Hsu, T., & Tzang, B. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2010.04.049 · Cited by 70 · see citing works
Kumarasinghe, N., Beveridge, N. J., Gardiner, E. J., Scott, R. J., Yasawardene, S. G., Perera, A., Mendis, J., Suriyakumara, K., Schall, U., & Tooney, P. A. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000035 · Cited by 70 · see citing works
Fragile X mental retardation protein levels are decreased in major psychiatric disorders
Fatemi, S. H., Kneeland, R. E., Liesch, S. B., & Folsom, T. D. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.07.017 · Cited by 69 · 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
Self-citationRibbe, K., Friedrichs, H., Begemann, M., Grube, S., Papiol, S., Kästner, A., Gerchen, M. F., Ackermann, V., Tarami, A., Treitz, A., et al. (2010) · BMC Psychiatry · doi:10.1186/1471-244x-10-91 · Cited by 61 · see citing works
Self-citationAli, F. T., El-Azeem, E. M. A., Hamed, M. A., Ali, M. A. M., Abdel-Kader, N. M., & Hassan, E. A. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.01.016 · Cited by 55 · see citing works
Structural Diversity and Extreme Stability of Unimolecular Oxytricha nova Telomeric G-Quadruplex
Lee, J. Y., Yoon, J., Kihm, H. W., & Kim, D. S. (2008) · Biochemistry · doi:10.1021/bi702013d · Cited by 54 · see citing works
Niedringhaus, M. S., Chen, X., Dzakpasu, R., & Conant, K. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042631 · Cited by 53 · see citing works
Kovács, T., Kelemen, O., & Kéri, S. (2013) · Psychiatry Research · doi:10.1016/j.psychres.2012.12.022 · Cited by 53 · see citing works
Nishida, Y., Pachulska‐Wieczorek, K., Błaszczyk, L., Saha, A., Gumna, J., Garfinkel, D. J., & Purzycka, K. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv695 · Cited by 44 · see citing works
Self-citationAccumulated common variants in the broader fragile X gene family modulate autistic phenotypes
Stepniak, B., Kästner, A., Poggi, G., Mitjans, M., Begemann, M., Hartmann, A. M., der Auwera, S. V., Sananbenesi, F., Krueger‐Burg, D., Matuszko, G., et al. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201505696 · Cited by 40 · see citing works
Self-citationExploring Ty1 retrotransposon RNA structure within virus-like particles
Purzycka, K. J., Łęgiewicz, M., Matsuda, E., Eizentstat, L. D., Lusvarghi, S., Saha, A., Grice, S. F. J. L., & Garfinkel, D. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks983 · Cited by 36 · see citing works
Self-citationRibbe, K. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.100 · Cited by 34 · see citing works
Huang, Q. B., Purzycka, K. J., Lusvarghi, S., Li, D., LeGrice, S. F. J., & Boeke, J. D. (2013) · RNA · doi:10.1261/rna.035535.112 · Cited by 33 · see citing works
Self-citationMMPs: a novel drug target for schizophrenia
Chopra, K., Baveja, A., & Kuhad, A. (2014) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2014.957672 · Cited by 32 · see citing works
Radyushkin, K., El-Kordi, A., Boretius, S., Vega, S. C., Ronnenberg, A., Reim, K., Bickeböller, H., Frahm, J., Brose, N., & Ehrenreich, H. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00590.x · Cited by 31 · see citing works
Self-citationThe in vitro loose dimer structure and rearrangements of the HIV-2 leader RNA
Purzycka, K. J., Pachulska‐Wieczorek, K., & Adamiak, R. W. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr385 · Cited by 31 · see citing works
Self-citationHan, H., He, X., Tang, J., Liu, W., Liu, K., Zhang, J., Wang, X., Xu, Y., & Chen, X. (2011) · Psychiatry Research · doi:10.1016/j.psychres.2011.04.026 · Cited by 22 · see citing works
The matrix domain contributes to the nucleic acid chaperone activity of HIV-2 Gag
Pachulska‐Wieczorek, K., Błaszczyk, L., Biesiada, M., Adamiak, R. W., & Purzycka, K. J. (2016) · Retrovirology · doi:10.1186/s12977-016-0245-1 · Cited by 20 · see citing works
Self-citationPachulska‐Wieczorek, K. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl373 · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
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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
Self-citationThe 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
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
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Mayne, P., & Burne, T. H. J. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.01.003 · Cited by 162 · see citing works
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Testa, D., Prochiantz, A., & Nardo, A. A. D. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.09.011 · Cited by 141 · see citing works
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Davis, J. K., & Broadie, K. S. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.07.008 · Cited by 118 · see citing works
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Zhang, Y., Gao, X., Bai, X., Yao, S., Chang, Y., & Gao, G. (2022) · Translational Neurodegeneration · doi:10.1186/s40035-022-00313-1 · Cited by 79 · see citing works
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Laguesse, S., & Dorit Ron, A. (2019) · The Neuroscientist · doi:10.1177/1073858419853236 · Cited by 59 · see citing works
Bijata, M., Bączyńska, E., Müller, F. E., Bijata, K., Masternak, J., Krzystyniak, A., Szewczyk, B., Siwiec, M., Antoniuk, S., Roszkowska, M., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110532 · Cited by 55 · see citing works
Self-citationBączyńska, E., Pels, K. K., Basu, S., Włodarczyk, J., & Ruszczycki, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084053 · Cited by 47 · 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
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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
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
Kudo, N., Yamamori, H., Ishima, T., Nemoto, K., Yasuda, Y., Fujimoto, M., Azechi, H., Niitsu, T., Numata, S., Ikeda, M., et al. (2020) · Neuropsychopharmacology Reports · doi:10.1002/npr2.12098 · Cited by 24 · 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
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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
Self-citationYin, H., Du, X., Li, Q., Pan, Z., Wu, W., Liu, H., & Liu, H. (2019) · Animals · doi:10.3390/ani9110905 · Cited by 17 · see citing works
Psychosocial Stress Induces Schizophrenia-Like Behavior in Mice With Reduced MMP-9 Activity
Vafadari, B., Mitra, S., Stefaniuk, M., & Kaczmarek, L. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00195 · Cited by 16 · see citing works
Self-citationDendritic spines and their role in the pathogenesis of neurodevelopmental and neurological disorders
Akhgari, A., Michel, T. M., & Vafaee, M. S. (2024) · Reviews in the Neurosciences · doi:10.1515/revneuro-2023-0151 · Cited by 14 · see citing works
Dysregulation of Synaptic Plasticity Markers in Schizophrenia
Keshri, N., & Nandeesha, H. (2022) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-022-01068-2 · Cited by 11 · see citing works
Filho, A. J. M. C., Mottin, M., Lós, D. B., Andrade, C. H., & Macêdo, D. S. (2022) · Biochimie · doi:10.1016/j.biochi.2022.07.015 · Cited by 11 · see citing works
Kaczmarek, L. (2018) · Postępy Biochemii · doi:10.18388/pb.2018_119 · Cited by 11 · see citing works
Self-citationLi, X., Wang, X., Yang, Y., Zhou, J., Wu, X., Zhao, J., Zhang, J., Guo, X., Shao, M., Song, M., et al. (2024) · Schizophrenia · doi:10.1038/s41537-024-00494-w · Cited by 10 · see citing works
Matusiak, M., Oziębło, D., Ołdak, M., Rejmak, E., Kaczmarek, L., Skarzynski, P. H., & Skarżyńśki, H. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02732-7 · Cited by 9 · see citing works
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Alemany-Navarro, M., Cruz, R., Real, E., Segalàs, C., Bertolín, S., Baenas, I., Domènech, L., Rabionet, R., Carracedo, Á., Menchón, J. M., et al. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.01.161 · Cited by 8 · see citing works
Xia, Q.-R., Zhang, C., Liang, J., & Xu, Y. (2019) · International journal of psychiatry in clinical practice · doi:10.1080/13651501.2019.1581895 · Cited by 7 · see citing works
Gao, J., Tang, X., Kang, J., Xie, C., Yu, M., Sha, W., Wang, X., Zhang, X., Zhang, X., & Yi, H. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2018.10.005 · Cited by 5 · see citing works
Lee, Y., Hsiao, C., Lin, F., Jan, J., Chou, Y.-C., Lin, Y.-Y., Chen, C.-K., Lam, K.-K., & Hsiao, G. (2018) · Mediators of Inflammation · doi:10.1155/2018/9541459 · Cited by 5 · see citing works
Markiewicz, R., Markiewicz-Gospodarek, A., Dobrowolska, B. B., Bojar, I., & Łoza, B. (2023) · Annals of Agricultural and Environmental Medicine · doi:10.26444/aaem/163327 · Cited by 4 · see citing works
Zhang, Y., Huang, M., Duan, R., Huang, W., & Tan, Z. (2025) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2025.118287 · Cited by 3 · see citing works
Alterations in the plasma concentrations of BDNF, proBDNF, and MMP-9 in patients with schizophrenia
Liang, Y., Pan, H., Yang, Z., Yu, C., Jiang, T., Li, Y., Yu, H., Qiu, M., & Zhang, S. (2025) · European journal of medical research · doi:10.1186/s40001-025-03153-7 · Cited by 3 · see citing works
Bai, S.-Y., Zeng, D.-Y., Ouyang, M., Zeng, Y., Tan, W., & Xu, L. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1393536 · Cited by 3 · see citing works
Abolghasemi, M., Daneshmandpour, Y., Poursaei, E., Jamshidi, J., Baradaran, B., Shanehbandi, D., Kazeminasab, S., & Emamalizadeh, B. (2020) · Meta Gene · doi:10.1016/j.mgene.2020.100810 · Cited by 2 · see citing works
A Drosophila screen of schizophrenia genes highlights neural and glial MMPs in neuronal remodeling
Keret, S., Meltzer, H., Marmor‐Kollet, N., & Schuldiner, O. (2025) · Life Science Alliance · doi:10.26508/lsa.202503504 · Cited by 1 · see citing works
Keret, S., Meltzer, H., Marmor‐Kollet, N., & Schuldiner, O. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.01.616025
Lcn2 deficiency leads to social impairments independent of maternal immune activationPreprint
Pękała, M., Zawiślak, S., Romanis, S., Nader, K., Cabaj, A., Madecka, A., Puścian, A., Knapska, E., Pawlak, R., Kaczmarek, L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.27.661499
Self-citationKeshri, N., Nandeesha, H., Menon, V., & Rajappa, M. (2026) · Indian Journal of Psychological Medicine · doi:10.1177/02537176251409364
Lcn2 deficiency leads to long-lasting social impairments independent of maternal immune activation
Pekala, M., Zawiślak, S., Romanis, S., Nader, K., Dzwonek, J., Cabaj, A., Madecka, A., Puścian, A., Knapska, E., Pawlak, R., et al. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03742-1
Self-citation
- Authors
- Lepeta, K., Purzycka, K. J., Pachulska‐Wieczorek, K., Mitjans, M., Begemann, M., Vafadari, B., Bijata, K., Adamiak, R. W., Ehrenreich, H., Dziembowska, M., & Kaczmarek, L.
- Affiliations
- Institute of Bioorganic Chemistry, Polish Academy of Sciences (PL)
- Nanoscale Microscopy and Molecular Physiology of the Brain Cluster of Excellence 171 — DFG Research Center 103 (DE)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Institute of Biochemistry and Biophysics, Polish Academy of Sciences (PL)
- Corresponding author
- Ehrenreich, Hannelore
- Dziembowska, Magdalena
- Kaczmarek, Leszek
- ORCID
- Venue
- EMBO Molecular Medicine
- Published
- 2017-06-16
- Volume
- 9
- Issue
- 8
- Pages
- 1100-1116
- ISSN
- 1757-4676 (ISSN-L)
- 1757-4684
- PMC
- PMC5538295
- OpenAlex
- W2624795293
- Cited by
- 39
- References
- 76
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 5 · 2021: 1 · 2020: 5 · 2019: 6 · 2018: 8 · 2017: 1
- FWCI
- 4.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- EMBO Molecular Medicine (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- GRO (submittedVersion)
- Funders
- EXTRABRAIN 7th Framework Marie Curie European Union Initial Training Network
- Polish Ministry of Science and Higher Education (UMOWA Nr 2948/7.PR/2013/2)
- Fundacja na rzecz Nauki Polskiej (TEAM Grant)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- schizophrenia, MMP-9, single nucleotide polymorphisms, 3' untranslated region, FMRP, dendritic spine morphology, synaptic plasticity, delusional symptoms, genotype-phenotype correlation
- MeSH terms
- Adolescent, Adult, Aged, Animals, Cells, Cultured, Chronic Disease, Disease Models, Animal, Female, Humans, Male, Middle Aged, Neurons, Nucleic Acid Conformation, Protein Binding, RNA, Messenger, Schizophrenia, Paranoid, Synapses, 3' Untranslated Regions, Polymorphism, Single Nucleotide, Matrix Metalloproteinase 9, Mice, Fragile X Messenger Ribonucleoprotein 1, Young Adult, Genetic Association Studies
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