Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations

Abstract A major goal in the field of transcriptional regulation is the mapping of changes in the binding of transcription factors to the resultant changes in gene expression. Recently, methods for measuring chromatin accessibility have enabled us to measure changes in accessibility across the genom...

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Main Authors: Karun Kiani, Eric M Sanford, Yogesh Goyal, Arjun Raj
Format: Article
Language:English
Published: Springer Nature 2022-09-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.202210979
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author Karun Kiani
Eric M Sanford
Yogesh Goyal
Arjun Raj
author_facet Karun Kiani
Eric M Sanford
Yogesh Goyal
Arjun Raj
author_sort Karun Kiani
collection DOAJ
description Abstract A major goal in the field of transcriptional regulation is the mapping of changes in the binding of transcription factors to the resultant changes in gene expression. Recently, methods for measuring chromatin accessibility have enabled us to measure changes in accessibility across the genome, which are thought to correspond to transcription factor‐binding events. In concert with RNA‐sequencing, these data in principle enable such mappings; however, few studies have looked at their concordance over short‐duration treatments with specific perturbations. Here, we used tandem, bulk ATAC‐seq, and RNA‐seq measurements from MCF‐7 breast carcinoma cells to systematically evaluate the concordance between changes in accessibility and changes in expression in response to retinoic acid and TGF‐β. We found two classes of genes whose expression showed a significant change: those that showed some changes in the accessibility of nearby chromatin, and those that showed virtually no change despite strong changes in expression. The peaks associated with genes in the former group had lower baseline accessibility prior to exposure to signal. Focusing the analysis specifically on peaks with motifs for transcription factors associated with retinoic acid and TGF‐β signaling did not reduce the lack of correspondence. Analysis of paired chromatin accessibility and gene expression data from distinct paths along the hematopoietic differentiation trajectory showed a much stronger correspondence, suggesting that the multifactorial biological processes associated with differentiation may lead to changes in chromatin accessibility that reflect rather than driving altered transcriptional status. Together, these results show many gene expression changes can happen independently of changes in the accessibility of local chromatin in the context of a single‐factor perturbation.
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spelling doaj-art-65c7f98ab5a945fb99fbcef6dff68b022025-08-20T03:43:34ZengSpringer NatureMolecular Systems Biology1744-42922022-09-0118911710.15252/msb.202210979Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbationsKarun Kiani0Eric M Sanford1Yogesh Goyal2Arjun Raj3Genetics and Epigenetics, Cell and Molecular Biology Graduate Group, Perelman School of Medicine, University of PennsylvaniaGenomics and Computational Biology Graduate Group, Perelman School of Medicine, University of PennsylvaniaDepartment of Bioengineering, School of Engineering and Applied Sciences, University of PennsylvaniaDepartment of Bioengineering, School of Engineering and Applied Sciences, University of PennsylvaniaAbstract A major goal in the field of transcriptional regulation is the mapping of changes in the binding of transcription factors to the resultant changes in gene expression. Recently, methods for measuring chromatin accessibility have enabled us to measure changes in accessibility across the genome, which are thought to correspond to transcription factor‐binding events. In concert with RNA‐sequencing, these data in principle enable such mappings; however, few studies have looked at their concordance over short‐duration treatments with specific perturbations. Here, we used tandem, bulk ATAC‐seq, and RNA‐seq measurements from MCF‐7 breast carcinoma cells to systematically evaluate the concordance between changes in accessibility and changes in expression in response to retinoic acid and TGF‐β. We found two classes of genes whose expression showed a significant change: those that showed some changes in the accessibility of nearby chromatin, and those that showed virtually no change despite strong changes in expression. The peaks associated with genes in the former group had lower baseline accessibility prior to exposure to signal. Focusing the analysis specifically on peaks with motifs for transcription factors associated with retinoic acid and TGF‐β signaling did not reduce the lack of correspondence. Analysis of paired chromatin accessibility and gene expression data from distinct paths along the hematopoietic differentiation trajectory showed a much stronger correspondence, suggesting that the multifactorial biological processes associated with differentiation may lead to changes in chromatin accessibility that reflect rather than driving altered transcriptional status. Together, these results show many gene expression changes can happen independently of changes in the accessibility of local chromatin in the context of a single‐factor perturbation.https://doi.org/10.15252/msb.202210979chromatin accessibilitygene regulationmulti‐omics integrationRNA‐seq and ATAC‐seq concordancesignal response
spellingShingle Karun Kiani
Eric M Sanford
Yogesh Goyal
Arjun Raj
Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
Molecular Systems Biology
chromatin accessibility
gene regulation
multi‐omics integration
RNA‐seq and ATAC‐seq concordance
signal response
title Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
title_full Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
title_fullStr Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
title_full_unstemmed Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
title_short Changes in chromatin accessibility are not concordant with transcriptional changes for single‐factor perturbations
title_sort changes in chromatin accessibility are not concordant with transcriptional changes for single factor perturbations
topic chromatin accessibility
gene regulation
multi‐omics integration
RNA‐seq and ATAC‐seq concordance
signal response
url https://doi.org/10.15252/msb.202210979
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AT ericmsanford changesinchromatinaccessibilityarenotconcordantwithtranscriptionalchangesforsinglefactorperturbations
AT yogeshgoyal changesinchromatinaccessibilityarenotconcordantwithtranscriptionalchangesforsinglefactorperturbations
AT arjunraj changesinchromatinaccessibilityarenotconcordantwithtranscriptionalchangesforsinglefactorperturbations