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...

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Main Authors: Claire Armstrong, Victor J. Passanisi, Humza M. Ashraf, Sabrina L. Spencer
Format: Article
Language:English
Published: Elsevier 2023-07-01
Series:Cell Reports
Subjects:
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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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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AT humzamashraf cyclinecdk2andfeedbackfromsolublehistoneproteinregulatethesphaseburstofhistonebiosynthesis
AT sabrinalspencer cyclinecdk2andfeedbackfromsolublehistoneproteinregulatethesphaseburstofhistonebiosynthesis