Function and regulation of transcription factors during mitosis-to-G1 transition

During cell division, drastic cellular changes characteristic of mitosis result in the inactivation of the transcriptional machinery, and global downregulation of transcription. Sequence-specific transcription factors (TFs) have thus been considered mere bystanders, devoid of any regulatory function...

Full description

Bibliographic Details
Main Authors: Mário A. F. Soares, Raquel A. Oliveira, Diogo S. Castro
Format: Article
Language:English
Published: The Royal Society 2022-06-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.220062
_version_ 1797974513185456128
author Mário A. F. Soares
Raquel A. Oliveira
Diogo S. Castro
author_facet Mário A. F. Soares
Raquel A. Oliveira
Diogo S. Castro
author_sort Mário A. F. Soares
collection DOAJ
description During cell division, drastic cellular changes characteristic of mitosis result in the inactivation of the transcriptional machinery, and global downregulation of transcription. Sequence-specific transcription factors (TFs) have thus been considered mere bystanders, devoid of any regulatory function during mitosis. This view changed significantly in recent years, upon the conclusion that many TFs associate with condensed chromosomes during cell division, even occupying a fraction of their genomic target sites in mitotic chromatin. This finding was at the origin of the concept of mitotic bookmarking by TFs, proposed as a mechanism to propagate gene regulatory information across cell divisions, by facilitating the reactivation of specific bookmarked genes. While the underlying mechanisms and biological significance of this model remain elusive, recent developments in this fast-moving field have cast new light into TF activity during mitosis, beyond a bookmarking role. Here, we start by reviewing the most recent findings on the complex nature of TF–chromatin interactions during mitosis, and on mechanisms that may regulate them. Next, and in light of recent reports describing how transcription is reinitiated in temporally distinct waves during mitosis-to-G1 transition, we explore how TFs may contribute to defining this hierarchical gene expression process. Finally, we discuss how TF activity during mitotic exit may impact the acquisition of cell identity upon cell division, and propose a model that integrates dynamic changes in TF–chromatin interactions during this cell-cycle period, with the execution of cell-fate decisions.
first_indexed 2024-04-11T04:20:58Z
format Article
id doaj.art-b2c0e16bd8c64f9b92c914e26e07d702
institution Directory Open Access Journal
issn 2046-2441
language English
last_indexed 2024-04-11T04:20:58Z
publishDate 2022-06-01
publisher The Royal Society
record_format Article
series Open Biology
spelling doaj.art-b2c0e16bd8c64f9b92c914e26e07d7022022-12-30T17:14:13ZengThe Royal SocietyOpen Biology2046-24412022-06-0112610.1098/rsob.220062Function and regulation of transcription factors during mitosis-to-G1 transitionMário A. F. Soares0Raquel A. Oliveira1Diogo S. Castro2i3S Instituto de Investigação e Inovação em Saúde, IBMC Instituto de Biologia Molecular e Celular, Universidade do Porto, 4200-135 Porto, PortugalInstituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugali3S Instituto de Investigação e Inovação em Saúde, IBMC Instituto de Biologia Molecular e Celular, Universidade do Porto, 4200-135 Porto, PortugalDuring cell division, drastic cellular changes characteristic of mitosis result in the inactivation of the transcriptional machinery, and global downregulation of transcription. Sequence-specific transcription factors (TFs) have thus been considered mere bystanders, devoid of any regulatory function during mitosis. This view changed significantly in recent years, upon the conclusion that many TFs associate with condensed chromosomes during cell division, even occupying a fraction of their genomic target sites in mitotic chromatin. This finding was at the origin of the concept of mitotic bookmarking by TFs, proposed as a mechanism to propagate gene regulatory information across cell divisions, by facilitating the reactivation of specific bookmarked genes. While the underlying mechanisms and biological significance of this model remain elusive, recent developments in this fast-moving field have cast new light into TF activity during mitosis, beyond a bookmarking role. Here, we start by reviewing the most recent findings on the complex nature of TF–chromatin interactions during mitosis, and on mechanisms that may regulate them. Next, and in light of recent reports describing how transcription is reinitiated in temporally distinct waves during mitosis-to-G1 transition, we explore how TFs may contribute to defining this hierarchical gene expression process. Finally, we discuss how TF activity during mitotic exit may impact the acquisition of cell identity upon cell division, and propose a model that integrates dynamic changes in TF–chromatin interactions during this cell-cycle period, with the execution of cell-fate decisions.https://royalsocietypublishing.org/doi/10.1098/rsob.220062transcription factormitotic bookmarkingmitosis-to-G1 transitionchromatinelectrostatic interactionssequence-specific binding
spellingShingle Mário A. F. Soares
Raquel A. Oliveira
Diogo S. Castro
Function and regulation of transcription factors during mitosis-to-G1 transition
Open Biology
transcription factor
mitotic bookmarking
mitosis-to-G1 transition
chromatin
electrostatic interactions
sequence-specific binding
title Function and regulation of transcription factors during mitosis-to-G1 transition
title_full Function and regulation of transcription factors during mitosis-to-G1 transition
title_fullStr Function and regulation of transcription factors during mitosis-to-G1 transition
title_full_unstemmed Function and regulation of transcription factors during mitosis-to-G1 transition
title_short Function and regulation of transcription factors during mitosis-to-G1 transition
title_sort function and regulation of transcription factors during mitosis to g1 transition
topic transcription factor
mitotic bookmarking
mitosis-to-G1 transition
chromatin
electrostatic interactions
sequence-specific binding
url https://royalsocietypublishing.org/doi/10.1098/rsob.220062
work_keys_str_mv AT marioafsoares functionandregulationoftranscriptionfactorsduringmitosistog1transition
AT raquelaoliveira functionandregulationoftranscriptionfactorsduringmitosistog1transition
AT diogoscastro functionandregulationoftranscriptionfactorsduringmitosistog1transition