MSK1 regulates transcriptional induction of Arc/Arg3.1 in response to neurotrophins

Christopher Hunter; Judit Remenyi; Sonia A. L.  Corrêa; Lucy Privitera; Kathleen Reyskens; Kirsty Martin; Rachel Toth; Bruno Frenguelli; John Arthur

doi:10.1002/2211-5463.12232

MSK1 regulates transcriptional induction of Arc/Arg3.1 in response to neurotrophins

Christopher Hunter, Judit Remenyi, Sonia A. L. Corrêa, Lucy Privitera, Kathleen Reyskens, Kirsty Martin, Rachel Toth, Bruno Frenguelli, John Arthur (Lead / Corresponding author)

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Abstract

The immediate early gene activity-regulated cytoskeletal protein (Arc)/Arg3.1 and the neurotrophin brain-derived neurotrophic factor (BDNF) play important roles in synaptic plasticity and learning and memory in the mammalian brain. However, the mechanisms by which BDNF regulates the expression of Arc/Arg3.1 are unclear. In this study, we show that BDNF acts via the ERK1/2 pathway to activate the nuclear kinase mitogen- and stress-activated protein kinase 1 (MSK1). MSK1 then induces Arc/Arg3.1 expression via the phosphorylation of histone H3 at the Arc/Arg3.1 promoter. MSK1 can also phosphorylate the transcription factor cyclic-AMP response element-binding protein (CREB) on Ser133. However, this is not required for BDNF-induced Arc.Arg3.1 transcription as a Ser133Ala knockin mutation had no effect on Arc/Arg3.1 induction. In parallel, ERK1/2 directly activates Arc/Arg3.1 mRNA transcription via at least one serum response element on the promoter, which bind a complex of the Serum Response Factor (SRF) and a Ternary Complex Factor (TCF).

Original language	English
Pages (from-to)	821-834
Number of pages	14
Journal	FEBS Open Bio
Volume	7
Issue number	6
Early online date	20 Apr 2017
DOIs	https://doi.org/10.1002/2211-5463.12232
Publication status	Published - 5 Jun 2017

Keywords

Arc-Arg3.1
BDNF
CREB
glutamate
histone H3
MSK1
neurotrophins
NMDA

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10.1002/2211-5463.12232Licence: CC BY

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© 2017 The Authors. Published by FEBS Press and John Wiley & Sons Ltd.This is an open access article under the terms of the Creative Commons Attribution License, which permits use,distribution and reproduction in any medium, provided the original work is properly cited.
Final published version, 755 KBLicence: CC BY

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@article{c442c9f79b5c40f0a8f63d724fa88ba9,

title = "MSK1 regulates transcriptional induction of Arc/Arg3.1 in response to neurotrophins",

abstract = "The immediate early gene activity-regulated cytoskeletal protein (Arc)/Arg3.1 and the neurotrophin brain-derived neurotrophic factor (BDNF) play important roles in synaptic plasticity and learning and memory in the mammalian brain. However, the mechanisms by which BDNF regulates the expression of Arc/Arg3.1 are unclear. In this study, we show that BDNF acts via the ERK1/2 pathway to activate the nuclear kinase mitogen- and stress-activated protein kinase 1 (MSK1). MSK1 then induces Arc/Arg3.1 expression via the phosphorylation of histone H3 at the Arc/Arg3.1 promoter. MSK1 can also phosphorylate the transcription factor cyclic-AMP response element-binding protein (CREB) on Ser133. However, this is not required for BDNF-induced Arc.Arg3.1 transcription as a Ser133Ala knockin mutation had no effect on Arc/Arg3.1 induction. In parallel, ERK1/2 directly activates Arc/Arg3.1 mRNA transcription via at least one serum response element on the promoter, which bind a complex of the Serum Response Factor (SRF) and a Ternary Complex Factor (TCF).",

keywords = "Arc-Arg3.1, BDNF, CREB, glutamate, histone H3, MSK1, neurotrophins, NMDA",

author = "Christopher Hunter and Judit Remenyi and Corr{\^e}a, {Sonia A. L.} and Lucy Privitera and Kathleen Reyskens and Kirsty Martin and Rachel Toth and Bruno Frenguelli and John Arthur",

note = "This work was supported by grants from the Wellcome Trust, BBSRC, MRC and WPH Charitable Trust.",

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T1 - MSK1 regulates transcriptional induction of Arc/Arg3.1 in response to neurotrophins

AU - Hunter, Christopher

AU - Remenyi, Judit

AU - Corrêa, Sonia A. L.

AU - Privitera, Lucy

AU - Reyskens, Kathleen

AU - Martin, Kirsty

AU - Toth, Rachel

AU - Frenguelli, Bruno

AU - Arthur, John

N1 - This work was supported by grants from the Wellcome Trust, BBSRC, MRC and WPH Charitable Trust.

PY - 2017/6/5

Y1 - 2017/6/5

N2 - The immediate early gene activity-regulated cytoskeletal protein (Arc)/Arg3.1 and the neurotrophin brain-derived neurotrophic factor (BDNF) play important roles in synaptic plasticity and learning and memory in the mammalian brain. However, the mechanisms by which BDNF regulates the expression of Arc/Arg3.1 are unclear. In this study, we show that BDNF acts via the ERK1/2 pathway to activate the nuclear kinase mitogen- and stress-activated protein kinase 1 (MSK1). MSK1 then induces Arc/Arg3.1 expression via the phosphorylation of histone H3 at the Arc/Arg3.1 promoter. MSK1 can also phosphorylate the transcription factor cyclic-AMP response element-binding protein (CREB) on Ser133. However, this is not required for BDNF-induced Arc.Arg3.1 transcription as a Ser133Ala knockin mutation had no effect on Arc/Arg3.1 induction. In parallel, ERK1/2 directly activates Arc/Arg3.1 mRNA transcription via at least one serum response element on the promoter, which bind a complex of the Serum Response Factor (SRF) and a Ternary Complex Factor (TCF).

AB - The immediate early gene activity-regulated cytoskeletal protein (Arc)/Arg3.1 and the neurotrophin brain-derived neurotrophic factor (BDNF) play important roles in synaptic plasticity and learning and memory in the mammalian brain. However, the mechanisms by which BDNF regulates the expression of Arc/Arg3.1 are unclear. In this study, we show that BDNF acts via the ERK1/2 pathway to activate the nuclear kinase mitogen- and stress-activated protein kinase 1 (MSK1). MSK1 then induces Arc/Arg3.1 expression via the phosphorylation of histone H3 at the Arc/Arg3.1 promoter. MSK1 can also phosphorylate the transcription factor cyclic-AMP response element-binding protein (CREB) on Ser133. However, this is not required for BDNF-induced Arc.Arg3.1 transcription as a Ser133Ala knockin mutation had no effect on Arc/Arg3.1 induction. In parallel, ERK1/2 directly activates Arc/Arg3.1 mRNA transcription via at least one serum response element on the promoter, which bind a complex of the Serum Response Factor (SRF) and a Ternary Complex Factor (TCF).

KW - Arc-Arg3.1

KW - BDNF

KW - CREB

KW - glutamate

KW - histone H3

KW - MSK1

KW - neurotrophins

KW - NMDA

U2 - 10.1002/2211-5463.12232

DO - 10.1002/2211-5463.12232

M3 - Article

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EP - 834

JO - FEBS Open Bio

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IS - 6

ER -

MSK1 regulates transcriptional induction of Arc/Arg3.1 in response to neurotrophins

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