Mild membrane depolarization in neurons induces immediate early gene transcription and acutely subdues responses to a successive stimulus

Mild membrane depolarization in neurons induces immediate early gene transcription and acutely subdues responses to a successive stimulus

Immediate early genes (IEGs) are transcribed in response to neuronal activity from sensory stimulation during multiple adaptive processes in the brain. The transcriptional profile of IEGs is indicative of the duration of neuronal activity, but its sensitivity to the strength of depolarization remain...

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Published in:The Journal of biological chemistry Vol. 298; no. 9; p. 102278
Main Authors: Rienecker, Kira D.A., Poston, Robert G., Segales, Joshua S., Finholm, Isabelle W., Sono, Morgan H., Munteanu, Sorina J., Ghaninejad-Esfahani, Mina, Rejepova, Ayna, Tejeda-Garibay, Susana, Wickman, Kevin, Marron Fernandez de Velasco, Ezequiel, Thayer, Stanley A., Saha, Ramendra N.
Format: Journal Article
Language:English
Published: Elsevier Inc 01-09-2022
American Society for Biochemistry and Molecular Biology
Subjects:
immediate early genes
intrinsic excitability
membrane depolarization
neuronal activity
transcription
transcription
DMSO
intrinsic excitability
FP
K
rIEG
CHX
TBS-T
CREB
KCl
immediate early genes
TTX
Bic
4AP
[Ca2+]i
PMA
neuronal activity
MEA
IEG
ACSF
MAPK
membrane depolarization
NMDAR
pERK
RRID
ERK
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Summary:Immediate early genes (IEGs) are transcribed in response to neuronal activity from sensory stimulation during multiple adaptive processes in the brain. The transcriptional profile of IEGs is indicative of the duration of neuronal activity, but its sensitivity to the strength of depolarization remains unknown. Also unknown is whether activity history of graded potential changes influence future neuronal activity. In this work with dissociated rat cortical neurons, we found that mild depolarization—mediated by elevated extracellular potassium (K+)—induces a wide array of rapid IEGs and transiently depresses transcriptional and signaling responses to a successive stimulus. This latter effect was independent of de novo transcription, translation, and signaling via calcineurin or mitogen-activated protein kinase. Furthermore, as measured by multiple electrode arrays and calcium imaging, mild depolarization acutely subdues subsequent spontaneous and bicuculline-evoked activity via calcium- and N-methyl-d-aspartate receptor–dependent mechanisms. Collectively, this work suggests that a recent history of graded potential changes acutely depress neuronal intrinsic properties and subsequent responses. Such effects may have several potential downstream implications, including reducing signal-to-noise ratio during synaptic plasticity processes.
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ISSN:0021-9258
1083-351X
DOI:10.1016/j.jbc.2022.102278