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Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae

The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by...

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Autores principales: Tsochatzidou, Maria, Malliarou, Maria, Papanikolaou, Nikolas, Roca, Joaquim, Nikolaou, Christoforos
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449599/
https://www.ncbi.nlm.nih.gov/pubmed/28369650
http://dx.doi.org/10.1093/nar/gkx198
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author Tsochatzidou, Maria
Malliarou, Maria
Papanikolaou, Nikolas
Roca, Joaquim
Nikolaou, Christoforos
author_facet Tsochatzidou, Maria
Malliarou, Maria
Papanikolaou, Nikolas
Roca, Joaquim
Nikolaou, Christoforos
author_sort Tsochatzidou, Maria
collection PubMed
description The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). By analyzing a genome-wide transcription run-on experiment upon thermal inactivation of topoII in Saccharomyces cerevisiae we were able to define 116 gene clusters of consistent response (either positive or negative) to topological stress. A comprehensive analysis of these topologically co-regulated gene clusters reveals pronounced preferences regarding their functional, regulatory and structural attributes. Genes that negatively respond to topological stress, are positioned in gene-dense pericentromeric regions, are more conserved and associated to essential functions, while upregulated gene clusters are preferentially located in the gene-sparse nuclear periphery, associated with secondary functions and under complex regulatory control. We propose that genome architecture evolves with a core of essential genes occupying a compact genomic ‘old town’, whereas more recently acquired, condition-specific genes tend to be located in a more spacious ‘suburban’ genomic periphery.
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spelling pubmed-54495992017-06-05 Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae Tsochatzidou, Maria Malliarou, Maria Papanikolaou, Nikolas Roca, Joaquim Nikolaou, Christoforos Nucleic Acids Res Gene regulation, Chromatin and Epigenetics The eukaryotic genome evolves under the dual constraint of maintaining coordinated gene transcription and performing effective DNA replication and cell division, the coupling of which brings about inevitable DNA topological tension. DNA supercoiling is resolved and, in some cases, even harnessed by the genome through the function of DNA topoisomerases, as has been shown in the concurrent transcriptional activation and suppression of genes upon transient deactivation of topoisomerase II (topoII). By analyzing a genome-wide transcription run-on experiment upon thermal inactivation of topoII in Saccharomyces cerevisiae we were able to define 116 gene clusters of consistent response (either positive or negative) to topological stress. A comprehensive analysis of these topologically co-regulated gene clusters reveals pronounced preferences regarding their functional, regulatory and structural attributes. Genes that negatively respond to topological stress, are positioned in gene-dense pericentromeric regions, are more conserved and associated to essential functions, while upregulated gene clusters are preferentially located in the gene-sparse nuclear periphery, associated with secondary functions and under complex regulatory control. We propose that genome architecture evolves with a core of essential genes occupying a compact genomic ‘old town’, whereas more recently acquired, condition-specific genes tend to be located in a more spacious ‘suburban’ genomic periphery. Oxford University Press 2017-06-02 2017-03-23 /pmc/articles/PMC5449599/ /pubmed/28369650 http://dx.doi.org/10.1093/nar/gkx198 Text en © The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Gene regulation, Chromatin and Epigenetics
Tsochatzidou, Maria
Malliarou, Maria
Papanikolaou, Nikolas
Roca, Joaquim
Nikolaou, Christoforos
Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title_full Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title_fullStr Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title_full_unstemmed Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title_short Genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of Saccharomyces cerevisiae
title_sort genome urbanization: clusters of topologically co-regulated genes delineate functional compartments in the genome of saccharomyces cerevisiae
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5449599/
https://www.ncbi.nlm.nih.gov/pubmed/28369650
http://dx.doi.org/10.1093/nar/gkx198
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