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The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number

Centrioles are submicron-scale, barrel-shaped organelles typically found in pairs, and play important roles in ciliogenesis and bipolar spindle assembly. In general, successful execution of centriole-dependent processes is highly reliant on the ability of the cell to stringently control centriole nu...

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Autores principales: Iyer, Jyoti, Gentry, Lindsey K., Bergwell, Mary, Smith, Amy, Guagliardo, Sarah, Kropp, Peter A., Sankaralingam, Prabhu, Liu, Yan, Spooner, Eric, Bowerman, Bruce, O’Connell, Kevin F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9009770/
https://www.ncbi.nlm.nih.gov/pubmed/35377871
http://dx.doi.org/10.1371/journal.pgen.1009799
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author Iyer, Jyoti
Gentry, Lindsey K.
Bergwell, Mary
Smith, Amy
Guagliardo, Sarah
Kropp, Peter A.
Sankaralingam, Prabhu
Liu, Yan
Spooner, Eric
Bowerman, Bruce
O’Connell, Kevin F.
author_facet Iyer, Jyoti
Gentry, Lindsey K.
Bergwell, Mary
Smith, Amy
Guagliardo, Sarah
Kropp, Peter A.
Sankaralingam, Prabhu
Liu, Yan
Spooner, Eric
Bowerman, Bruce
O’Connell, Kevin F.
author_sort Iyer, Jyoti
collection PubMed
description Centrioles are submicron-scale, barrel-shaped organelles typically found in pairs, and play important roles in ciliogenesis and bipolar spindle assembly. In general, successful execution of centriole-dependent processes is highly reliant on the ability of the cell to stringently control centriole number. This in turn is mainly achieved through the precise duplication of centrioles during each S phase. Aberrations in centriole duplication disrupt spindle assembly and cilia-based signaling and have been linked to cancer, primary microcephaly and a variety of growth disorders. Studies aimed at understanding how centriole duplication is controlled have mainly focused on the post-translational regulation of two key components of this pathway: the master regulatory kinase ZYG-1/Plk4 and the scaffold component SAS-6. In contrast, how transcriptional control mechanisms might contribute to this process have not been well explored. Here we show that the chromatin remodeling protein CHD-1 contributes to the regulation of centriole duplication in the C. elegans embryo. Specifically, we find that loss of CHD-1 or inactivation of its ATPase activity can restore embryonic viability and centriole duplication to a strain expressing insufficient ZYG-1 activity. Interestingly, loss of CHD-1 is associated with increases in the levels of two ZYG-1-binding partners: SPD-2, the centriole receptor for ZYG-1 and SAS-6. Finally, we explore transcriptional regulatory networks governing centriole duplication and find that CHD-1 and a second transcription factor, EFL-1/DPL-1 cooperate to down regulate expression of CDK-2, which in turn promotes SAS-6 protein levels. Disruption of this regulatory network results in the overexpression of SAS-6 and the production of extra centrioles.
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spelling pubmed-90097702022-04-15 The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number Iyer, Jyoti Gentry, Lindsey K. Bergwell, Mary Smith, Amy Guagliardo, Sarah Kropp, Peter A. Sankaralingam, Prabhu Liu, Yan Spooner, Eric Bowerman, Bruce O’Connell, Kevin F. PLoS Genet Research Article Centrioles are submicron-scale, barrel-shaped organelles typically found in pairs, and play important roles in ciliogenesis and bipolar spindle assembly. In general, successful execution of centriole-dependent processes is highly reliant on the ability of the cell to stringently control centriole number. This in turn is mainly achieved through the precise duplication of centrioles during each S phase. Aberrations in centriole duplication disrupt spindle assembly and cilia-based signaling and have been linked to cancer, primary microcephaly and a variety of growth disorders. Studies aimed at understanding how centriole duplication is controlled have mainly focused on the post-translational regulation of two key components of this pathway: the master regulatory kinase ZYG-1/Plk4 and the scaffold component SAS-6. In contrast, how transcriptional control mechanisms might contribute to this process have not been well explored. Here we show that the chromatin remodeling protein CHD-1 contributes to the regulation of centriole duplication in the C. elegans embryo. Specifically, we find that loss of CHD-1 or inactivation of its ATPase activity can restore embryonic viability and centriole duplication to a strain expressing insufficient ZYG-1 activity. Interestingly, loss of CHD-1 is associated with increases in the levels of two ZYG-1-binding partners: SPD-2, the centriole receptor for ZYG-1 and SAS-6. Finally, we explore transcriptional regulatory networks governing centriole duplication and find that CHD-1 and a second transcription factor, EFL-1/DPL-1 cooperate to down regulate expression of CDK-2, which in turn promotes SAS-6 protein levels. Disruption of this regulatory network results in the overexpression of SAS-6 and the production of extra centrioles. Public Library of Science 2022-04-04 /pmc/articles/PMC9009770/ /pubmed/35377871 http://dx.doi.org/10.1371/journal.pgen.1009799 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Iyer, Jyoti
Gentry, Lindsey K.
Bergwell, Mary
Smith, Amy
Guagliardo, Sarah
Kropp, Peter A.
Sankaralingam, Prabhu
Liu, Yan
Spooner, Eric
Bowerman, Bruce
O’Connell, Kevin F.
The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title_full The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title_fullStr The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title_full_unstemmed The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title_short The chromatin remodeling protein CHD-1 and the EFL-1/DPL-1 transcription factor cooperatively down regulate CDK-2 to control SAS-6 levels and centriole number
title_sort chromatin remodeling protein chd-1 and the efl-1/dpl-1 transcription factor cooperatively down regulate cdk-2 to control sas-6 levels and centriole number
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9009770/
https://www.ncbi.nlm.nih.gov/pubmed/35377871
http://dx.doi.org/10.1371/journal.pgen.1009799
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