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A high-content screen reveals new regulators of nuclear membrane stability

Nuclear membrane rupture is a physiological response to multiple in vivo processes, such as cell migration, that can cause extensive genome instability and upregulate invasive and inflammatory pathways. However, the underlying molecular mechanisms of rupture are unclear and few regulators have been...

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Autores principales: Gunn, Amanda L., Yashchenko, Artem I., Dubrulle, Julien, Johnson, Jodiene, Hatch, Emily M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312541/
https://www.ncbi.nlm.nih.gov/pubmed/37398267
http://dx.doi.org/10.1101/2023.05.30.542944
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author Gunn, Amanda L.
Yashchenko, Artem I.
Dubrulle, Julien
Johnson, Jodiene
Hatch, Emily M.
author_facet Gunn, Amanda L.
Yashchenko, Artem I.
Dubrulle, Julien
Johnson, Jodiene
Hatch, Emily M.
author_sort Gunn, Amanda L.
collection PubMed
description Nuclear membrane rupture is a physiological response to multiple in vivo processes, such as cell migration, that can cause extensive genome instability and upregulate invasive and inflammatory pathways. However, the underlying molecular mechanisms of rupture are unclear and few regulators have been identified. In this study, we developed a reporter that is size excluded from re-compartmentalization following nuclear rupture events. This allows for robust detection of factors influencing nuclear integrity in fixed cells. We combined this with an automated image analysis pipeline in a high-content siRNA screen to identify new proteins that both increase and decrease nuclear rupture frequency in cancer cells. Pathway analysis identified an enrichment of nuclear membrane and ER factors in our hits and we demonstrate that one of these, the protein phosphatase CTDNEP1, is required for nuclear stability. Further analysis of known rupture contributors, including a newly developed automated quantitative analysis of nuclear lamina gaps, strongly suggests that CTDNEP1 acts in a new pathway. Our findings provide new insights into the molecular mechanism of nuclear rupture and define a highly adaptable program for rupture analysis that removes a substantial barrier to new discoveries in the field.
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spelling pubmed-103125412023-07-01 A high-content screen reveals new regulators of nuclear membrane stability Gunn, Amanda L. Yashchenko, Artem I. Dubrulle, Julien Johnson, Jodiene Hatch, Emily M. bioRxiv Article Nuclear membrane rupture is a physiological response to multiple in vivo processes, such as cell migration, that can cause extensive genome instability and upregulate invasive and inflammatory pathways. However, the underlying molecular mechanisms of rupture are unclear and few regulators have been identified. In this study, we developed a reporter that is size excluded from re-compartmentalization following nuclear rupture events. This allows for robust detection of factors influencing nuclear integrity in fixed cells. We combined this with an automated image analysis pipeline in a high-content siRNA screen to identify new proteins that both increase and decrease nuclear rupture frequency in cancer cells. Pathway analysis identified an enrichment of nuclear membrane and ER factors in our hits and we demonstrate that one of these, the protein phosphatase CTDNEP1, is required for nuclear stability. Further analysis of known rupture contributors, including a newly developed automated quantitative analysis of nuclear lamina gaps, strongly suggests that CTDNEP1 acts in a new pathway. Our findings provide new insights into the molecular mechanism of nuclear rupture and define a highly adaptable program for rupture analysis that removes a substantial barrier to new discoveries in the field. Cold Spring Harbor Laboratory 2023-09-10 /pmc/articles/PMC10312541/ /pubmed/37398267 http://dx.doi.org/10.1101/2023.05.30.542944 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Gunn, Amanda L.
Yashchenko, Artem I.
Dubrulle, Julien
Johnson, Jodiene
Hatch, Emily M.
A high-content screen reveals new regulators of nuclear membrane stability
title A high-content screen reveals new regulators of nuclear membrane stability
title_full A high-content screen reveals new regulators of nuclear membrane stability
title_fullStr A high-content screen reveals new regulators of nuclear membrane stability
title_full_unstemmed A high-content screen reveals new regulators of nuclear membrane stability
title_short A high-content screen reveals new regulators of nuclear membrane stability
title_sort high-content screen reveals new regulators of nuclear membrane stability
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312541/
https://www.ncbi.nlm.nih.gov/pubmed/37398267
http://dx.doi.org/10.1101/2023.05.30.542944
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