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A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases

In fast-transcribing prokaryotic genes, such as an rrn gene in Escherichia coli, many RNA polymerases (RNAPs) transcribe the DNA simultaneously. Active elongation of RNAPs is often interrupted by pauses, which has been observed to cause RNAP traffic jams; yet some studies indicate that elongation se...

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Autores principales: Heberling, Tamra, Davis, Lisa, Gedeon, Jakub, Morgan, Charles, Gedeon, Tomáš
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4982667/
https://www.ncbi.nlm.nih.gov/pubmed/27517607
http://dx.doi.org/10.1371/journal.pcbi.1005069
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author Heberling, Tamra
Davis, Lisa
Gedeon, Jakub
Morgan, Charles
Gedeon, Tomáš
author_facet Heberling, Tamra
Davis, Lisa
Gedeon, Jakub
Morgan, Charles
Gedeon, Tomáš
author_sort Heberling, Tamra
collection PubMed
description In fast-transcribing prokaryotic genes, such as an rrn gene in Escherichia coli, many RNA polymerases (RNAPs) transcribe the DNA simultaneously. Active elongation of RNAPs is often interrupted by pauses, which has been observed to cause RNAP traffic jams; yet some studies indicate that elongation seems to be faster in the presence of multiple RNAPs than elongation by a single RNAP. We propose that an interaction between RNAPs via the torque produced by RNAP motion on helically twisted DNA can explain this apparent paradox. We have incorporated the torque mechanism into a stochastic model and simulated transcription both with and without torque. Simulation results illustrate that the torque causes shorter pause durations and fewer collisions between polymerases. Our results suggest that the torsional interaction of RNAPs is an important mechanism in maintaining fast transcription times, and that transcription should be viewed as a cooperative group effort by multiple polymerases.
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spelling pubmed-49826672016-08-29 A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases Heberling, Tamra Davis, Lisa Gedeon, Jakub Morgan, Charles Gedeon, Tomáš PLoS Comput Biol Research Article In fast-transcribing prokaryotic genes, such as an rrn gene in Escherichia coli, many RNA polymerases (RNAPs) transcribe the DNA simultaneously. Active elongation of RNAPs is often interrupted by pauses, which has been observed to cause RNAP traffic jams; yet some studies indicate that elongation seems to be faster in the presence of multiple RNAPs than elongation by a single RNAP. We propose that an interaction between RNAPs via the torque produced by RNAP motion on helically twisted DNA can explain this apparent paradox. We have incorporated the torque mechanism into a stochastic model and simulated transcription both with and without torque. Simulation results illustrate that the torque causes shorter pause durations and fewer collisions between polymerases. Our results suggest that the torsional interaction of RNAPs is an important mechanism in maintaining fast transcription times, and that transcription should be viewed as a cooperative group effort by multiple polymerases. Public Library of Science 2016-08-12 /pmc/articles/PMC4982667/ /pubmed/27517607 http://dx.doi.org/10.1371/journal.pcbi.1005069 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Heberling, Tamra
Davis, Lisa
Gedeon, Jakub
Morgan, Charles
Gedeon, Tomáš
A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title_full A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title_fullStr A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title_full_unstemmed A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title_short A Mechanistic Model for Cooperative Behavior of Co-transcribing RNA Polymerases
title_sort mechanistic model for cooperative behavior of co-transcribing rna polymerases
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4982667/
https://www.ncbi.nlm.nih.gov/pubmed/27517607
http://dx.doi.org/10.1371/journal.pcbi.1005069
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