Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-Fos pathway

Kuzniewska, Bozena; Rejmak, Emilia; Malik, Anna R.; Jaworski, Jacek; Kaczmarek, Leszek; Kalita, Katarzyna

doi:10.1128/mcb.00008-13

Cited by 82Nerve injury and regenerationProtease and Inhibitor MechanismsNeurogenesis and neuroplasticity mechanisms

Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-Fos pathway

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Kuzniewska, Bozena, Rejmak, Emilia, Malik, Anna R., Jaworski, Jacek, Kaczmarek, Leszek, Kalita, Katarzyna·2013·Molecular and Cellular Biology

DOI 10.1128/mcb.00008-13PMC PMC3648073

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Abstract

Brain-derived neurotrophic factor (BDNF) plays a pivotal role in the regulation of the transcription of genes that encode proplasticity proteins. In the present study, we provide evidence that stimulation of rat primary cortical neurons with BDNF upregulates matrix metalloproteinase 9 (MMP-9) mRNA and protein levels and increases enzymatic activity. The BDNF-induced MMP-9 transcription was dependent on extracellular signal-regulated kinase 1/2 (ERK1/2) pathway and c-Fos expression. Overexpression of AP-1 dimers in neurons led to MMP-9 promoter activation, with the most potent being those that contained c-Fos, whereas knockdown of endogenous c-Fos by small hairpin RNA (shRNA) reduced BDNF-mediated MMP-9 transcription. Additionally, mutation of the proximal AP-1 binding site in the MMP-9 promoter inhibited the activation of MMP-9 transcription. BDNF stimulation of neurons induced binding of endogenous c-Fos to the proximal MMP-9 promoter region. Furthermore, as the c-Fos gene is a known target of serum response factor (SRF), we investigated whether SRF contributes to MMP-9 transcription. Inhibition of SRF and its cofactors by either overexpression of dominant negative mutants or shRNA decreased MMP-9 promoter activation. In contrast, MMP-9 transcription was not dependent on CREB activity. Finally, we showed that neuronal activity stimulates MMP-9 transcription in a tyrosine kinase receptor B (TrkB)-dependent manner.

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Expression of COL1A2, MMP9, and TGFB2 is regulated by SRF and MRTFs.
“The expression of COL1A2, MMP9, and TGFB2 is under the regulation of serum response factor (SRF) and myocardin-related transcription factors (MRTFs) (Gilles et al., 2009; Haak et al., 2014; Kuzniewska et al., 2013; Li et al., 2012).”
From Enhancer-associated aortic valve stenosis risk locus 1p21.2 alters NFATC2 binding site and promotes fibrogenesis (2021) · cites this paper as Kuzniewska et al., 2013
The Discussion (page unavailable) states that SRF and its cofactors MKL1 and MKL2 regulate MMP-9 transcription in neurons. The paper does not establish the same regulation for COL1A2 or TGFB2, so it supports only the MMP9 portion of the sentence. (LLM, conf=0.88)
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BDNF can increase expression of extracellular metalloproteinases and induces ApoER2 cleavage through binding TrkB receptors.
“This neurotrophin can increase the expression of extracellular metalloproteinases (46) and induces ApoER2 cleavage through binding TrkB receptors (47) (Fig. 2B, 5).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [46]

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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
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Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses
Wasser, C. R., & Herz, J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.766782 · Cited by 111 · see citing works
Behavioral and neurochemical characterization of TrkB-dependent mechanisms of agomelatine in glucocorticoid receptor-impaired mice
Boulle, F., Velthuis, H., Koedam, K., Steinbusch, H. W., van den Hove, D. L. A., Kenis, G., Gabriel, C., Mocaer, E., Franc, B., Rognan, D., et al. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.003 · Cited by 24 · see citing works
Enhancer-associated aortic valve stenosis risk locus 1p21.2 alters NFATC2 binding site and promotes fibrogenesis
Chignon, A., Rosa, M., Boulanger, M.-C., Argaud, D., Devillers, R., Bon-Baret, V., Mkannez, G., Li, Z., Rufiange, A., Gaudreault, N., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102241 · Cited by 18 · see citing works

Two pathways for serum regulation of the c-fos serum response element require specific sequence elements and a minimal domain of serum response factor.
Johansen, F. E., & Prywes, R. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.9.5920 · Cited by 141 · see citing works
Full Promoter Sequence of Human Early Growth Response Factor-1 (Egr-1): Demonstration of a Fifth Functional Serum Response Element
Schwachtgen, J.-L., Campbell, C. J., & Braddock, M. (2000) · DNA sequence · doi:10.3109/10425170009015615 · Cited by 46 · see citing works
Serum response factor (c-fos serum response element-binding transcription factor; SRF)
(2011) · Science-Business eXchange · doi:10.1038/scibx.2011.313
The Tissue-Specific Transcription Factor Pit-1/GHF-1 Binds to the c-fos Serum Response Element and Activates c-fos Transcription
Gaiddon, C., de Tapia, M., & Loeffler, J. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.5.0275 · Cited by 35 · see citing works
Fibroblast Growth Factor Receptor 3 Gene: Regulation by Serum Response Factor
Reinhold, M. I., McEwen, D. G., & Naski, M. C. (2003) · Molecular Endocrinology · doi:10.1210/me.2003-0312 · Cited by 9 · see citing works

Authors: Kuzniewska, B., Rejmak, E., Malik, A. R., Jaworski, J., Kaczmarek, L., & Kalita, K.
Affiliations: Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences
Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
International Institute of Molecular and Cell Biology (PL)
ORCID: Rejmak, Emilia
Malik, Anna R.
Jaworski, Jacek
Kaczmarek, Leszek
Kalita, Katarzyna
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 2013-06
Volume: 33
Issue: 11
Pages: 2149-2162
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.00008-13
PMC: PMC3648073
OpenAlex: W2160573720
Cited by: 82
References: 70
Citations by year: 2026: 5 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 7 · 2020: 9 · 2019: 5 · 2018: 8 · 2017: 2 · 2016: 8 · 2015: 11 · 2014: 7 · 2013: 1
FWCI: 4.41
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission (230992)
Fundacja na rzecz Nauki Polskiej
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: brain-derived neurotrophic factor, MMP-9, serum response factor, c-fos, AP-1 transcription factor, ERK signaling, cortical neurons, TrkB receptor, CREB, neuronal activity, transcriptional regulation
MeSH terms: Animals, Base Sequence, Bicuculline, Binding Sites, Cells, Cultured, Molecular Sequence Data, Neurons, Promoter Regions, Genetic, Gene Expression Regulation, Enzymologic, Proto-Oncogene Proteins c-fos, Rats, Wistar, Cyclic AMP Response Element-Binding Protein, Transcription Factor AP-1, Brain-Derived Neurotrophic Factor, Matrix Metalloproteinase 9, Serum Response Factor, RNA, Small Interfering, Mitogen-Activated Protein Kinase 3, Rats

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Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-Fos pathway

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