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Comparative analysis reveals genomic features of stress-induced transcriptional readthrough.

Transcription is a highly regulated process, and stress-induced changes in gene transcription have been shown to play a major role in stress responses and adaptation. Genome-wide studies reveal prevalent transcription beyond known protein-coding gene loci, generating a variety of RNA classes, most o... Full description

Journal Title: Proceedings of the National Academy of Sciences of the United States of America October 3, 2017, Vol.114(40), pp.E8362-E8371
Main Author: Vilborg, Anna
Other Authors: Sabath, Niv , Wiesel, Yuval , Nathans, Jenny , Levy-Adam, Flonia , Yario, Therese A , Steitz, Joan A , Shalgi, Reut
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1711120114
Link: http://search.proquest.com/docview/1941099202/?pq-origsite=primo
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title: Comparative analysis reveals genomic features of stress-induced transcriptional readthrough.
format: Article
creator:
  • Vilborg, Anna
  • Sabath, Niv
  • Wiesel, Yuval
  • Nathans, Jenny
  • Levy-Adam, Flonia
  • Yario, Therese A
  • Steitz, Joan A
  • Shalgi, Reut
subjects:
  • Animals–Methods
  • Gene Expression Profiling–Methods
  • Gene Expression Regulation–Methods
  • Genome–Methods
  • Genomics–Methods
  • Heat-Shock Response–Methods
  • Mice–Methods
  • NIH 3t3 Cells–Methods
  • Osmotic Pressure–Methods
  • Oxidative Stress–Methods
  • Transcription, Genetic–Methods
  • Stress Response
  • Transcription Regulation
  • Transcriptional Readthrough
ispartof: Proceedings of the National Academy of Sciences of the United States of America, October 3, 2017, Vol.114(40), pp.E8362-E8371
description: Transcription is a highly regulated process, and stress-induced changes in gene transcription have been shown to play a major role in stress responses and adaptation. Genome-wide studies reveal prevalent transcription beyond known protein-coding gene loci, generating a variety of RNA classes, most of unknown function. One such class, termed downstream of gene-containing transcripts (DoGs), was reported to result from transcriptional readthrough upon osmotic stress in human cells. However, how widespread the readthrough phenomenon is, and what its causes and consequences are, remain elusive. Here we present a genome-wide mapping of transcriptional readthrough, using nuclear RNA-Seq, comparing heat shock, osmotic stress, and oxidative stress in NIH 3T3 mouse fibroblast cells. We observe massive induction of transcriptional readthrough, both in levels and length, under all stress conditions, with significant, yet not complete, overlap of readthrough-induced loci between different conditions. Importantly, our analyses suggest that stress-induced transcriptional readthrough is not a random failure process, but is rather differentially induced across different conditions. We explore potential regulators and find a role for HSF1 in the induction of a subset of heat shock-induced readthrough transcripts. Analysis of public datasets detected increases in polymerase II occupancy in DoG regions after heat shock, supporting our findings. Interestingly, DoGs tend to be produced in the vicinity of neighboring genes, leading to a marked increase in their antisense-generating potential. Finally, we examine genomic features of readthrough transcription and observe a unique chromatin signature typical of DoG-producing regions, suggesting that readthrough transcription is associated with the maintenance of an open chromatin state.
language: eng
source:
identifier: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1711120114
fulltext: fulltext
issn:
  • 10916490
  • 1091-6490
url: Link


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titleComparative analysis reveals genomic features of stress-induced transcriptional readthrough.
creatorVilborg, Anna ; Sabath, Niv ; Wiesel, Yuval ; Nathans, Jenny ; Levy-Adam, Flonia ; Yario, Therese A ; Steitz, Joan A ; Shalgi, Reut
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subjectAnimals–Methods ; Gene Expression Profiling–Methods ; Gene Expression Regulation–Methods ; Genome–Methods ; Genomics–Methods ; Heat-Shock Response–Methods ; Mice–Methods ; NIH 3t3 Cells–Methods ; Osmotic Pressure–Methods ; Oxidative Stress–Methods ; Transcription, Genetic–Methods ; Stress Response ; Transcription Regulation ; Transcriptional Readthrough
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descriptionTranscription is a highly regulated process, and stress-induced changes in gene transcription have been shown to play a major role in stress responses and adaptation. Genome-wide studies reveal prevalent transcription beyond known protein-coding gene loci, generating a variety of RNA classes, most of unknown function. One such class, termed downstream of gene-containing transcripts (DoGs), was reported to result from transcriptional readthrough upon osmotic stress in human cells. However, how widespread the readthrough phenomenon is, and what its causes and consequences are, remain elusive. Here we present a genome-wide mapping of transcriptional readthrough, using nuclear RNA-Seq, comparing heat shock, osmotic stress, and oxidative stress in NIH 3T3 mouse fibroblast cells. We observe massive induction of transcriptional readthrough, both in levels and length, under all stress conditions, with significant, yet not complete, overlap of readthrough-induced loci between different conditions. Importantly, our analyses suggest that stress-induced transcriptional readthrough is not a random failure process, but is rather differentially induced across different conditions. We explore potential regulators and find a role for HSF1 in the induction of a subset of heat shock-induced readthrough transcripts. Analysis of public datasets detected increases in polymerase II occupancy in DoG regions after heat shock, supporting our findings. Interestingly, DoGs tend to be produced in the vicinity of neighboring genes, leading to a marked increase in their antisense-generating potential. Finally, we examine genomic features of readthrough transcription and observe a unique chromatin signature typical of DoG-producing regions, suggesting that readthrough transcription is associated with the maintenance of an open chromatin state.
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