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Research Articles, Cellular/Molecular

Differential Regulation of the BDNF Gene in Cortical and Hippocampal Neurons

Eli-Eelika Esvald, Jürgen Tuvikene, Andra Moistus, Käthy Rannaste, Susann Kõomägi and Tõnis Timmusk
Journal of Neuroscience 7 December 2022, 42 (49) 9110-9128; DOI: https://doi.org/10.1523/JNEUROSCI.2535-21.2022
Eli-Eelika Esvald
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
2Protobios LLC, Tallinn 12618, Estonia
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Jürgen Tuvikene
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
2Protobios LLC, Tallinn 12618, Estonia
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Andra Moistus
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
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Käthy Rannaste
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
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Susann Kõomägi
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
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Tõnis Timmusk
1Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn 12618, Estonia
2Protobios LLC, Tallinn 12618, Estonia
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Abstract

Brain-derived neurotrophic factor (BDNF) is a widely expressed neurotrophin that supports the survival, differentiation, and signaling of various neuronal populations. Although it has been well described that expression of BDNF is strongly regulated by neuronal activity, little is known whether regulation of BDNF expression is similar in different brain regions. Here, we focused on this fundamental question using neuronal populations obtained from rat cerebral cortices and hippocampi of both sexes. First, we thoroughly characterized the role of the best-described regulators of BDNF gene - cAMP response element binding protein (CREB) family transcription factors, and show that activity-dependent BDNF expression depends more on CREB and the coactivators CREB binding protein (CBP) and CREB-regulated transcriptional coactivator 1 (CRTC1) in cortical than in hippocampal neurons. Our data also reveal an important role of CREB in the early induction of BDNF mRNA expression after neuronal activity and only modest contribution after prolonged neuronal activity. We further corroborated our findings at BDNF protein level. To determine the transcription factors regulating BDNF expression in these rat brain regions in addition to CREB family, we used in vitro DNA pulldown assay coupled with mass spectrometry, chromatin immunoprecipitation (ChIP), and bioinformatics, and propose a number of neurodevelopmentally important transcription factors, such as FOXP1, SATB2, RAI1, BCL11A, and TCF4 as brain region-specific regulators of BDNF expression. Together, our data reveal complicated brain region-specific fine-tuning of BDNF expression.

SIGNIFICANCE STATEMENT To date, majority of the research has focused on the regulation of brain-derived neurotrophic factor (BDNF) in the brain but much less is known whether the regulation of BDNF expression is universal in different brain regions and neuronal populations. Here, we report that the best described regulators of BDNF gene from the cAMP-response element binding protein (CREB) transcription factor family have a more profound role in the activity-dependent regulation of BDNF in cortex than in hippocampus. Our results indicate a brain region-specific fine tuning of BDNF expression. Moreover, we have used unbiased determination of novel regulators of the BDNF gene and report a number of neurodevelopmentally important transcription factors as novel potential regulators of the BDNF expression.

  • BDNF cortex
  • CREB
  • hippocampus
  • neuronal activity

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The Journal of Neuroscience: 42 (49)
Journal of Neuroscience
Vol. 42, Issue 49
7 Dec 2022
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Differential Regulation of the BDNF Gene in Cortical and Hippocampal Neurons
Eli-Eelika Esvald, Jürgen Tuvikene, Andra Moistus, Käthy Rannaste, Susann Kõomägi, Tõnis Timmusk
Journal of Neuroscience 7 December 2022, 42 (49) 9110-9128; DOI: 10.1523/JNEUROSCI.2535-21.2022

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Differential Regulation of the BDNF Gene in Cortical and Hippocampal Neurons
Eli-Eelika Esvald, Jürgen Tuvikene, Andra Moistus, Käthy Rannaste, Susann Kõomägi, Tõnis Timmusk
Journal of Neuroscience 7 December 2022, 42 (49) 9110-9128; DOI: 10.1523/JNEUROSCI.2535-21.2022
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Keywords

  • BDNF cortex
  • CREB
  • hippocampus
  • neuronal activity

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