FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1

Abstract Aging is characterized by changes in gene expression, some of which can drive deleterious cellular phenotypes and senescence. The transcriptional activation of senescence genes has been mainly attributed to epigenetic shifts, but the changes in chromatin accessibility and its underlying mec...

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Main Authors: Fábio J. Ferreira, Mafalda Galhardo, João M. Nogueira, Joana Teixeira, Elsa Logarinho, José Bessa
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-57503-4
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author Fábio J. Ferreira
Mafalda Galhardo
João M. Nogueira
Joana Teixeira
Elsa Logarinho
José Bessa
author_facet Fábio J. Ferreira
Mafalda Galhardo
João M. Nogueira
Joana Teixeira
Elsa Logarinho
José Bessa
author_sort Fábio J. Ferreira
collection DOAJ
description Abstract Aging is characterized by changes in gene expression, some of which can drive deleterious cellular phenotypes and senescence. The transcriptional activation of senescence genes has been mainly attributed to epigenetic shifts, but the changes in chromatin accessibility and its underlying mechanisms remain largely elusive in natural aging. Here, we profiled chromatin accessibility in human dermal fibroblasts (HDFs) from individuals with ages ranging from neonatal to octogenarian. We found that AP-1 binding motifs are prevalent in elderly-specific accessible chromatin regions while neonatal-specific regions are highly enriched for TEAD binding motifs. We further show that TEAD4 and FOXM1 share a conserved transcriptional regulatory landscape controlled by a not previously described and age-dependent enhancer that loses accessibility with aging and whose deletion drives senescence. Finally, we demonstrate that FOXM1 ectopic expression in elderly cells partially resets chromatin accessibility to a youthful state due to FOXM1’s repressive function on several members of the AP-1 complex, which is known to trigger the senescence transcriptional program. These results place FOXM1 at a top hierarchical level in chromatin remodeling required to prevent senescence.
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issn 2041-1723
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publishDate 2025-03-01
publisher Nature Portfolio
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series Nature Communications
spelling doaj-art-ecc82bf0e19a482e8436edff14d3598b2025-08-20T03:40:50ZengNature PortfolioNature Communications2041-17232025-03-0116111510.1038/s41467-025-57503-4FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1Fábio J. Ferreira0Mafalda Galhardo1João M. Nogueira2Joana Teixeira3Elsa Logarinho4José Bessa5i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Portoi3S - Instituto de Investigação e Inovação em Saúde, Universidade do Portoi3S - Instituto de Investigação e Inovação em Saúde, Universidade do Portoi3S - Instituto de Investigação e Inovação em Saúde, Universidade do Portoi3S - Instituto de Investigação e Inovação em Saúde, Universidade do Portoi3S - Instituto de Investigação e Inovação em Saúde, Universidade do PortoAbstract Aging is characterized by changes in gene expression, some of which can drive deleterious cellular phenotypes and senescence. The transcriptional activation of senescence genes has been mainly attributed to epigenetic shifts, but the changes in chromatin accessibility and its underlying mechanisms remain largely elusive in natural aging. Here, we profiled chromatin accessibility in human dermal fibroblasts (HDFs) from individuals with ages ranging from neonatal to octogenarian. We found that AP-1 binding motifs are prevalent in elderly-specific accessible chromatin regions while neonatal-specific regions are highly enriched for TEAD binding motifs. We further show that TEAD4 and FOXM1 share a conserved transcriptional regulatory landscape controlled by a not previously described and age-dependent enhancer that loses accessibility with aging and whose deletion drives senescence. Finally, we demonstrate that FOXM1 ectopic expression in elderly cells partially resets chromatin accessibility to a youthful state due to FOXM1’s repressive function on several members of the AP-1 complex, which is known to trigger the senescence transcriptional program. These results place FOXM1 at a top hierarchical level in chromatin remodeling required to prevent senescence.https://doi.org/10.1038/s41467-025-57503-4
spellingShingle Fábio J. Ferreira
Mafalda Galhardo
João M. Nogueira
Joana Teixeira
Elsa Logarinho
José Bessa
FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
Nature Communications
title FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
title_full FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
title_fullStr FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
title_full_unstemmed FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
title_short FOXM1 expression reverts aging chromatin profiles through repression of the senescence-associated pioneer factor AP-1
title_sort foxm1 expression reverts aging chromatin profiles through repression of the senescence associated pioneer factor ap 1
url https://doi.org/10.1038/s41467-025-57503-4
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