Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality

Summary: Despite the symmetrical structure of nucleosomes, in vitro studies have shown that transcription proceeds with different efficiency depending on the orientation of the DNA sequence around them. However, it is unclear whether this functional asymmetry is present in vivo and whether it could...

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Main Authors: Alicia García, Laura Durán, Mar Sánchez, Sara González, Rodrigo Santamaría, Francisco Antequera
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723016170
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author Alicia García
Laura Durán
Mar Sánchez
Sara González
Rodrigo Santamaría
Francisco Antequera
author_facet Alicia García
Laura Durán
Mar Sánchez
Sara González
Rodrigo Santamaría
Francisco Antequera
author_sort Alicia García
collection DOAJ
description Summary: Despite the symmetrical structure of nucleosomes, in vitro studies have shown that transcription proceeds with different efficiency depending on the orientation of the DNA sequence around them. However, it is unclear whether this functional asymmetry is present in vivo and whether it could regulate transcriptional directionality. Here, we report that the proximal and distal halves of nucleosomal DNA contribute differentially to nucleosome stability in the genome. In +1 nucleosomes, this asymmetry facilitates or hinders transcription depending on the orientation of its underlying DNA, and this difference is associated with an asymmetrical interaction between DNA and histones. These properties are encoded in the DNA signature of +1 nucleosomes, since its incorporation in the two orientations into downstream nucleosomes renders them asymmetrically accessible to MNase and inverts the balance between sense and antisense transcription. Altogether, our results show that nucleosomal DNA endows nucleosomes with asymmetrical properties that modulate the directionality of transcription.
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spelling doaj.art-75d51a40174e4e3d97626f15fdd078f62023-12-22T05:32:45ZengElsevierCell Reports2211-12472024-01-01431113605Asymmetrical nucleosomal DNA signatures regulate transcriptional directionalityAlicia García0Laura Durán1Mar Sánchez2Sara González3Rodrigo Santamaría4Francisco Antequera5Instituto de Biología Funcional y Genómica (IBFG), CSIC–Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, SpainInstituto de Biología Funcional y Genómica (IBFG), CSIC–Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, SpainInstituto de Biología Funcional y Genómica (IBFG), CSIC–Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, SpainInstituto de Biología Funcional y Genómica (IBFG), CSIC–Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, SpainDepartamento de Informática y Automática, Universidad de Salamanca/Facultad de Ciencias, Plaza de los Caídos s/n, 37007 Salamanca, SpainInstituto de Biología Funcional y Genómica (IBFG), CSIC–Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, Spain; Corresponding authorSummary: Despite the symmetrical structure of nucleosomes, in vitro studies have shown that transcription proceeds with different efficiency depending on the orientation of the DNA sequence around them. However, it is unclear whether this functional asymmetry is present in vivo and whether it could regulate transcriptional directionality. Here, we report that the proximal and distal halves of nucleosomal DNA contribute differentially to nucleosome stability in the genome. In +1 nucleosomes, this asymmetry facilitates or hinders transcription depending on the orientation of its underlying DNA, and this difference is associated with an asymmetrical interaction between DNA and histones. These properties are encoded in the DNA signature of +1 nucleosomes, since its incorporation in the two orientations into downstream nucleosomes renders them asymmetrically accessible to MNase and inverts the balance between sense and antisense transcription. Altogether, our results show that nucleosomal DNA endows nucleosomes with asymmetrical properties that modulate the directionality of transcription.http://www.sciencedirect.com/science/article/pii/S2211124723016170CP: Molecular biology
spellingShingle Alicia García
Laura Durán
Mar Sánchez
Sara González
Rodrigo Santamaría
Francisco Antequera
Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
Cell Reports
CP: Molecular biology
title Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
title_full Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
title_fullStr Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
title_full_unstemmed Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
title_short Asymmetrical nucleosomal DNA signatures regulate transcriptional directionality
title_sort asymmetrical nucleosomal dna signatures regulate transcriptional directionality
topic CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124723016170
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AT saragonzalez asymmetricalnucleosomaldnasignaturesregulatetranscriptionaldirectionality
AT rodrigosantamaria asymmetricalnucleosomaldnasignaturesregulatetranscriptionaldirectionality
AT franciscoantequera asymmetricalnucleosomaldnasignaturesregulatetranscriptionaldirectionality