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Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response

Dynamic regulation of gene expression via signal transduction pathways is of fundamental importance during many biological processes such as cell state transitioning, cell cycle progression and stress responses. In this study we used serum stimulation as a cell response paradigm to apply the nascent...

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Autores principales: Kirkconnell, Killeen S., Paulsen, Michelle T., Magnuson, Brian, Bedi, Karan, Ljungman, Mats
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4920201/
https://www.ncbi.nlm.nih.gov/pubmed/27230646
http://dx.doi.org/10.1242/bio.019323
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author Kirkconnell, Killeen S.
Paulsen, Michelle T.
Magnuson, Brian
Bedi, Karan
Ljungman, Mats
author_facet Kirkconnell, Killeen S.
Paulsen, Michelle T.
Magnuson, Brian
Bedi, Karan
Ljungman, Mats
author_sort Kirkconnell, Killeen S.
collection PubMed
description Dynamic regulation of gene expression via signal transduction pathways is of fundamental importance during many biological processes such as cell state transitioning, cell cycle progression and stress responses. In this study we used serum stimulation as a cell response paradigm to apply the nascent RNA Bru-seq technique in order to capture early dynamic changes in the nascent transcriptome. Our data provides an unprecedented view of the dynamics of genome-wide transcription during the first two hours of serum stimulation in human fibroblasts. While some genes showed sustained induction or repression, other genes showed transient or delayed responses. Surprisingly, the dynamic patterns of induction and suppression of response genes showed a high degree of similarity, suggesting that these opposite outcomes are triggered by a common set of signals. As expected, early response genes such as those encoding components of the AP-1 transcription factor and those involved in the circadian clock were immediately but transiently induced. Surprisingly, transcription of important DNA damage response genes and histone genes were rapidly repressed. We also show that RNA polymerase II accelerates as it transcribes large genes and this was independent of whether the gene was induced or not. These results provide a unique genome-wide depiction of dynamic patterns of transcription of serum response genes and demonstrate the utility of Bru-seq to comprehensively capture rapid and dynamic changes of the nascent transcriptome.
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spelling pubmed-49202012016-07-07 Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response Kirkconnell, Killeen S. Paulsen, Michelle T. Magnuson, Brian Bedi, Karan Ljungman, Mats Biol Open Research Article Dynamic regulation of gene expression via signal transduction pathways is of fundamental importance during many biological processes such as cell state transitioning, cell cycle progression and stress responses. In this study we used serum stimulation as a cell response paradigm to apply the nascent RNA Bru-seq technique in order to capture early dynamic changes in the nascent transcriptome. Our data provides an unprecedented view of the dynamics of genome-wide transcription during the first two hours of serum stimulation in human fibroblasts. While some genes showed sustained induction or repression, other genes showed transient or delayed responses. Surprisingly, the dynamic patterns of induction and suppression of response genes showed a high degree of similarity, suggesting that these opposite outcomes are triggered by a common set of signals. As expected, early response genes such as those encoding components of the AP-1 transcription factor and those involved in the circadian clock were immediately but transiently induced. Surprisingly, transcription of important DNA damage response genes and histone genes were rapidly repressed. We also show that RNA polymerase II accelerates as it transcribes large genes and this was independent of whether the gene was induced or not. These results provide a unique genome-wide depiction of dynamic patterns of transcription of serum response genes and demonstrate the utility of Bru-seq to comprehensively capture rapid and dynamic changes of the nascent transcriptome. The Company of Biologists Ltd 2016-05-26 /pmc/articles/PMC4920201/ /pubmed/27230646 http://dx.doi.org/10.1242/bio.019323 Text en © 2016. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Kirkconnell, Killeen S.
Paulsen, Michelle T.
Magnuson, Brian
Bedi, Karan
Ljungman, Mats
Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title_full Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title_fullStr Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title_full_unstemmed Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title_short Capturing the dynamic nascent transcriptome during acute cellular responses: The serum response
title_sort capturing the dynamic nascent transcriptome during acute cellular responses: the serum response
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4920201/
https://www.ncbi.nlm.nih.gov/pubmed/27230646
http://dx.doi.org/10.1242/bio.019323
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