Transcription factor expression is the main determinant of variability in gene co‐activity

Abstract Many genes are co‐expressed and form genomic domains of coordinated gene activity. However, the regulatory determinants of domain co‐activity remain unclear. Here, we leverage human individual variation in gene expression to characterize the co‐regulatory processes underlying domain co‐acti...

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Main Authors: Lucas van Duin, Robert Krautz, Sarah Rennie, Robin Andersson
Format: Article
Language:English
Published: Springer Nature 2023-05-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.202211392
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author Lucas van Duin
Robert Krautz
Sarah Rennie
Robin Andersson
author_facet Lucas van Duin
Robert Krautz
Sarah Rennie
Robin Andersson
author_sort Lucas van Duin
collection DOAJ
description Abstract Many genes are co‐expressed and form genomic domains of coordinated gene activity. However, the regulatory determinants of domain co‐activity remain unclear. Here, we leverage human individual variation in gene expression to characterize the co‐regulatory processes underlying domain co‐activity and systematically quantify their effect sizes. We employ transcriptional decomposition to extract from RNA expression data an expression component related to co‐activity revealed by genomic positioning. This strategy reveals close to 1,500 co‐activity domains, covering most expressed genes, of which the large majority are invariable across individuals. Focusing specifically on domains with high variability in co‐activity reveals that contained genes have a higher sharing of eQTLs, a higher variability in enhancer interactions, and an enrichment of binding by variably expressed transcription factors, compared to genes within non‐variable domains. Through careful quantification of the relative contributions of regulatory processes underlying co‐activity, we find transcription factor expression levels to be the main determinant of gene co‐activity. Our results indicate that distal trans effects contribute more than local genetic variation to individual variation in co‐activity domains.
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spelling doaj-art-c0ff0e72b3834be1a2a4a6dc42af6a372024-11-10T12:48:18ZengSpringer NatureMolecular Systems Biology1744-42922023-05-0119711710.15252/msb.202211392Transcription factor expression is the main determinant of variability in gene co‐activityLucas van Duin0Robert Krautz1Sarah Rennie2Robin Andersson3Section for Computational and RNA Biology, Department of Biology, University of CopenhagenSection for Computational and RNA Biology, Department of Biology, University of CopenhagenSection for Computational and RNA Biology, Department of Biology, University of CopenhagenSection for Computational and RNA Biology, Department of Biology, University of CopenhagenAbstract Many genes are co‐expressed and form genomic domains of coordinated gene activity. However, the regulatory determinants of domain co‐activity remain unclear. Here, we leverage human individual variation in gene expression to characterize the co‐regulatory processes underlying domain co‐activity and systematically quantify their effect sizes. We employ transcriptional decomposition to extract from RNA expression data an expression component related to co‐activity revealed by genomic positioning. This strategy reveals close to 1,500 co‐activity domains, covering most expressed genes, of which the large majority are invariable across individuals. Focusing specifically on domains with high variability in co‐activity reveals that contained genes have a higher sharing of eQTLs, a higher variability in enhancer interactions, and an enrichment of binding by variably expressed transcription factors, compared to genes within non‐variable domains. Through careful quantification of the relative contributions of regulatory processes underlying co‐activity, we find transcription factor expression levels to be the main determinant of gene co‐activity. Our results indicate that distal trans effects contribute more than local genetic variation to individual variation in co‐activity domains.https://doi.org/10.15252/msb.202211392co‐activity domainsco‐regulationgene regulationindividual variationtranscriptional decomposition
spellingShingle Lucas van Duin
Robert Krautz
Sarah Rennie
Robin Andersson
Transcription factor expression is the main determinant of variability in gene co‐activity
Molecular Systems Biology
co‐activity domains
co‐regulation
gene regulation
individual variation
transcriptional decomposition
title Transcription factor expression is the main determinant of variability in gene co‐activity
title_full Transcription factor expression is the main determinant of variability in gene co‐activity
title_fullStr Transcription factor expression is the main determinant of variability in gene co‐activity
title_full_unstemmed Transcription factor expression is the main determinant of variability in gene co‐activity
title_short Transcription factor expression is the main determinant of variability in gene co‐activity
title_sort transcription factor expression is the main determinant of variability in gene co activity
topic co‐activity domains
co‐regulation
gene regulation
individual variation
transcriptional decomposition
url https://doi.org/10.15252/msb.202211392
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AT robertkrautz transcriptionfactorexpressionisthemaindeterminantofvariabilityingenecoactivity
AT sarahrennie transcriptionfactorexpressionisthemaindeterminantofvariabilityingenecoactivity
AT robinandersson transcriptionfactorexpressionisthemaindeterminantofvariabilityingenecoactivity