E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells

Abstract While mitogenic signaling is known to regulate cell-cycle entry during the G1 phase, its function in the G2 phase remains elusive. Here we show that mitogenic signaling controls whether G2-arrested cells proceed through mitosis or undergo whole-genome duplication. Although mitogenic signali...

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Main Authors: Kibum Kim, Jessica Armand, Sungsoo Kim, Hee Won Yang
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62061-w
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author Kibum Kim
Jessica Armand
Sungsoo Kim
Hee Won Yang
author_facet Kibum Kim
Jessica Armand
Sungsoo Kim
Hee Won Yang
author_sort Kibum Kim
collection DOAJ
description Abstract While mitogenic signaling is known to regulate cell-cycle entry during the G1 phase, its function in the G2 phase remains elusive. Here we show that mitogenic signaling controls whether G2-arrested cells proceed through mitosis or undergo whole-genome duplication. Although mitogenic signaling is not required for the G2/M transition under normal conditions, it modulates E2F transcriptional activity via c-Myc. When G2 arrest occurs due to CDK4/6 and CDK2 suppression, E2F activity levels determine the status of APC/C inactivation and the CDK2-Rb feedback loop. Upon release from G2 arrest, cells maintaining APC/C inactivation promptly induce CDK2 activation and FoxM1 phosphorylation, driving mitotic entry. Conversely, APC/C reactivation degrades cyclin A and abolishes the CDK2-Rb loop, necessitating CDK4/6 activation for cell-cycle re-entry. This regulatory mechanism mirrors the G1-phase process, resulting in whole-genome duplication. In cancer cells, this process promotes genome instability and oncogene amplification, contributing to aggressive behavior. These findings reveal a previously unrecognized mitogen-dependent checkpoint that governs cell fate in the G2 phase.
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spelling doaj-art-cc586d8610f64a3a8d2f651a02d6deaa2025-08-20T03:43:16ZengNature PortfolioNature Communications2041-17232025-07-0116111310.1038/s41467-025-62061-wE2F activity determines mitosis versus whole-genome duplication in G2-arrested cellsKibum Kim0Jessica Armand1Sungsoo Kim2Hee Won Yang3Department of Pathology and Cell Biology, Columbia UniversityDepartment of Pathology and Cell Biology, Columbia UniversityDepartment of Pathology and Cell Biology, Columbia UniversityDepartment of Pathology and Cell Biology, Columbia UniversityAbstract While mitogenic signaling is known to regulate cell-cycle entry during the G1 phase, its function in the G2 phase remains elusive. Here we show that mitogenic signaling controls whether G2-arrested cells proceed through mitosis or undergo whole-genome duplication. Although mitogenic signaling is not required for the G2/M transition under normal conditions, it modulates E2F transcriptional activity via c-Myc. When G2 arrest occurs due to CDK4/6 and CDK2 suppression, E2F activity levels determine the status of APC/C inactivation and the CDK2-Rb feedback loop. Upon release from G2 arrest, cells maintaining APC/C inactivation promptly induce CDK2 activation and FoxM1 phosphorylation, driving mitotic entry. Conversely, APC/C reactivation degrades cyclin A and abolishes the CDK2-Rb loop, necessitating CDK4/6 activation for cell-cycle re-entry. This regulatory mechanism mirrors the G1-phase process, resulting in whole-genome duplication. In cancer cells, this process promotes genome instability and oncogene amplification, contributing to aggressive behavior. These findings reveal a previously unrecognized mitogen-dependent checkpoint that governs cell fate in the G2 phase.https://doi.org/10.1038/s41467-025-62061-w
spellingShingle Kibum Kim
Jessica Armand
Sungsoo Kim
Hee Won Yang
E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
Nature Communications
title E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
title_full E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
title_fullStr E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
title_full_unstemmed E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
title_short E2F activity determines mitosis versus whole-genome duplication in G2-arrested cells
title_sort e2f activity determines mitosis versus whole genome duplication in g2 arrested cells
url https://doi.org/10.1038/s41467-025-62061-w
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