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Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress

Insertion sequence elements (IS elements) are proposed to play major roles in shaping the genetic and phenotypic landscapes of prokaryotic cells. Recent evidence has raised the possibility that environmental stress conditions increase IS hopping into new sites, and often such hopping has the phenoty...

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Autores principales: Humayun, M. Zafri, Zhang, Zhongge, Butcher, Anna M., Moshayedi, Aref, Saier, Milton H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5493358/
https://www.ncbi.nlm.nih.gov/pubmed/28666002
http://dx.doi.org/10.1371/journal.pone.0180156
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author Humayun, M. Zafri
Zhang, Zhongge
Butcher, Anna M.
Moshayedi, Aref
Saier, Milton H.
author_facet Humayun, M. Zafri
Zhang, Zhongge
Butcher, Anna M.
Moshayedi, Aref
Saier, Milton H.
author_sort Humayun, M. Zafri
collection PubMed
description Insertion sequence elements (IS elements) are proposed to play major roles in shaping the genetic and phenotypic landscapes of prokaryotic cells. Recent evidence has raised the possibility that environmental stress conditions increase IS hopping into new sites, and often such hopping has the phenotypic effect of relieving the stress. Although stress-induced targeted mutations have been reported for a number of E. coli genes, the glpFK (glycerol utilization) and the cryptic bglGFB (β-glucoside utilization) systems are among the best characterized where the effects of IS insertion-mediated gene activation are well-characterized at the molecular level. In the glpFK system, starvation of cells incapable of utilizing glycerol leads to an IS5 insertion event that activates the glpFK operon, and enables glycerol utilization. In the case of the cryptic bglGFB operon, insertion of IS5 (and other IS elements) into a specific region in the bglG upstream sequence has the effect of activating the operon in both growing cells, and in starving cells. However, a major unanswered question in the glpFK system, the bgl system, as well as other examples, has been why the insertion events are promoted at specific locations, and how the specific stress condition (glycerol starvation for example) can be mechanistically linked to enhanced insertion at a specific locus. In this paper, we show that a specific DNA structural feature (superhelical stress-induced duplex destabilization, SIDD) is associated with “stress-induced” IS5 insertion in the glpFK, bglGFB, flhDC, fucAO and nfsB systems. We propose a speculative mechanistic model that links specific environmental conditions to the unmasking of an insertional hotspot in the glpFK system. We demonstrate that experimentally altering the predicted stability of a SIDD element in the nfsB gene significantly impacts IS5 insertion at its hotspot.
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spelling pubmed-54933582017-07-18 Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress Humayun, M. Zafri Zhang, Zhongge Butcher, Anna M. Moshayedi, Aref Saier, Milton H. PLoS One Research Article Insertion sequence elements (IS elements) are proposed to play major roles in shaping the genetic and phenotypic landscapes of prokaryotic cells. Recent evidence has raised the possibility that environmental stress conditions increase IS hopping into new sites, and often such hopping has the phenotypic effect of relieving the stress. Although stress-induced targeted mutations have been reported for a number of E. coli genes, the glpFK (glycerol utilization) and the cryptic bglGFB (β-glucoside utilization) systems are among the best characterized where the effects of IS insertion-mediated gene activation are well-characterized at the molecular level. In the glpFK system, starvation of cells incapable of utilizing glycerol leads to an IS5 insertion event that activates the glpFK operon, and enables glycerol utilization. In the case of the cryptic bglGFB operon, insertion of IS5 (and other IS elements) into a specific region in the bglG upstream sequence has the effect of activating the operon in both growing cells, and in starving cells. However, a major unanswered question in the glpFK system, the bgl system, as well as other examples, has been why the insertion events are promoted at specific locations, and how the specific stress condition (glycerol starvation for example) can be mechanistically linked to enhanced insertion at a specific locus. In this paper, we show that a specific DNA structural feature (superhelical stress-induced duplex destabilization, SIDD) is associated with “stress-induced” IS5 insertion in the glpFK, bglGFB, flhDC, fucAO and nfsB systems. We propose a speculative mechanistic model that links specific environmental conditions to the unmasking of an insertional hotspot in the glpFK system. We demonstrate that experimentally altering the predicted stability of a SIDD element in the nfsB gene significantly impacts IS5 insertion at its hotspot. Public Library of Science 2017-06-30 /pmc/articles/PMC5493358/ /pubmed/28666002 http://dx.doi.org/10.1371/journal.pone.0180156 Text en © 2017 Humayun et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Humayun, M. Zafri
Zhang, Zhongge
Butcher, Anna M.
Moshayedi, Aref
Saier, Milton H.
Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title_full Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title_fullStr Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title_full_unstemmed Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title_short Hopping into a hot seat: Role of DNA structural features on IS5-mediated gene activation and inactivation under stress
title_sort hopping into a hot seat: role of dna structural features on is5-mediated gene activation and inactivation under stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5493358/
https://www.ncbi.nlm.nih.gov/pubmed/28666002
http://dx.doi.org/10.1371/journal.pone.0180156
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