Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis
Summary: Faithful DNA replication requires that cells fine-tune their histone pool in coordination with cell-cycle progression. Replication-dependent histone biosynthesis is initiated at a low level upon cell-cycle commitment, followed by a burst at the G1/S transition, but it remains unclear how ex...
Main Authors: | , , , |
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Format: | Article |
Language: | English |
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Elsevier
2023-07-01
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Series: | Cell Reports |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723007799 |
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author | Claire Armstrong Victor J. Passanisi Humza M. Ashraf Sabrina L. Spencer |
author_facet | Claire Armstrong Victor J. Passanisi Humza M. Ashraf Sabrina L. Spencer |
author_sort | Claire Armstrong |
collection | DOAJ |
description | Summary: Faithful DNA replication requires that cells fine-tune their histone pool in coordination with cell-cycle progression. Replication-dependent histone biosynthesis is initiated at a low level upon cell-cycle commitment, followed by a burst at the G1/S transition, but it remains unclear how exactly the cell regulates this burst in histone biosynthesis as DNA replication begins. Here, we use single-cell time-lapse imaging to elucidate the mechanisms by which cells modulate histone production during different phases of the cell cycle. We find that CDK2-mediated phosphorylation of NPAT at the restriction point triggers histone transcription, which results in a burst of histone mRNA precisely at the G1/S phase boundary. Excess soluble histone protein further modulates histone abundance by promoting the degradation of histone mRNA for the duration of S phase. Thus, cells regulate their histone production in strict coordination with cell-cycle progression by two distinct mechanisms acting in concert. |
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id | doaj.art-fd2a58a4570f4e79a13bb5f99d4a6445 |
institution | Directory Open Access Journal |
issn | 2211-1247 |
language | English |
last_indexed | 2024-03-13T00:28:37Z |
publishDate | 2023-07-01 |
publisher | Elsevier |
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series | Cell Reports |
spelling | doaj.art-fd2a58a4570f4e79a13bb5f99d4a64452023-07-11T04:06:20ZengElsevierCell Reports2211-12472023-07-01427112768Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesisClaire Armstrong0Victor J. Passanisi1Humza M. Ashraf2Sabrina L. Spencer3Department of Biochemistry, University of Colorado Boulder, Boulder, CO 80303, USA; BioFrontiers Institute, University of Colorado Boulder, Boulder, CO 80303, USADepartment of Biochemistry, University of Colorado Boulder, Boulder, CO 80303, USA; BioFrontiers Institute, University of Colorado Boulder, Boulder, CO 80303, USADepartment of Biochemistry, University of Colorado Boulder, Boulder, CO 80303, USA; BioFrontiers Institute, University of Colorado Boulder, Boulder, CO 80303, USADepartment of Biochemistry, University of Colorado Boulder, Boulder, CO 80303, USA; BioFrontiers Institute, University of Colorado Boulder, Boulder, CO 80303, USA; Corresponding authorSummary: Faithful DNA replication requires that cells fine-tune their histone pool in coordination with cell-cycle progression. Replication-dependent histone biosynthesis is initiated at a low level upon cell-cycle commitment, followed by a burst at the G1/S transition, but it remains unclear how exactly the cell regulates this burst in histone biosynthesis as DNA replication begins. Here, we use single-cell time-lapse imaging to elucidate the mechanisms by which cells modulate histone production during different phases of the cell cycle. We find that CDK2-mediated phosphorylation of NPAT at the restriction point triggers histone transcription, which results in a burst of histone mRNA precisely at the G1/S phase boundary. Excess soluble histone protein further modulates histone abundance by promoting the degradation of histone mRNA for the duration of S phase. Thus, cells regulate their histone production in strict coordination with cell-cycle progression by two distinct mechanisms acting in concert.http://www.sciencedirect.com/science/article/pii/S2211124723007799CP: Cell biologyCP: Molecular biology |
spellingShingle | Claire Armstrong Victor J. Passanisi Humza M. Ashraf Sabrina L. Spencer Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis Cell Reports CP: Cell biology CP: Molecular biology |
title | Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis |
title_full | Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis |
title_fullStr | Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis |
title_full_unstemmed | Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis |
title_short | Cyclin E/CDK2 and feedback from soluble histone protein regulate the S phase burst of histone biosynthesis |
title_sort | cyclin e cdk2 and feedback from soluble histone protein regulate the s phase burst of histone biosynthesis |
topic | CP: Cell biology CP: Molecular biology |
url | http://www.sciencedirect.com/science/article/pii/S2211124723007799 |
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