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Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling

The accumulation of prelamin A is linked to disruption of cellular homeostasis, tissue degeneration and aging. Its expression is implicated in compromised genome stability and increased levels of DNA damage, but to date there is no complete explanation for how prelamin A exerts its toxic effects. As...

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Autores principales: Cobb, Andrew M., Murray, Thomas V., Warren, Derek T., Liu, Yiwen, Shanahan, Catherine M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Taylor & Francis 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5120601/
https://www.ncbi.nlm.nih.gov/pubmed/27676213
http://dx.doi.org/10.1080/19491034.2016.1239685
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author Cobb, Andrew M.
Murray, Thomas V.
Warren, Derek T.
Liu, Yiwen
Shanahan, Catherine M.
author_facet Cobb, Andrew M.
Murray, Thomas V.
Warren, Derek T.
Liu, Yiwen
Shanahan, Catherine M.
author_sort Cobb, Andrew M.
collection PubMed
description The accumulation of prelamin A is linked to disruption of cellular homeostasis, tissue degeneration and aging. Its expression is implicated in compromised genome stability and increased levels of DNA damage, but to date there is no complete explanation for how prelamin A exerts its toxic effects. As the nuclear lamina is important for DNA replication we wanted to investigate the relationship between prelamin A expression and DNA replication fork stability. In this study we report that the expression of prelamin A in U2OS cells induced both mono-ubiquitination of proliferating cell nuclear antigen (PCNA) and subsequent induction of Pol η, two hallmarks of DNA replication fork stalling. Immunofluorescence microscopy revealed that cells expressing prelamin A presented with high levels of colocalisation between PCNA and γH2AX, indicating collapse of stalled DNA replication forks into DNA double-strand breaks. Subsequent protein-protein interaction assays showed prelamin A interacted with PCNA and that its presence mitigated interactions between PCNA and the mature nuclear lamina. Thus, we propose that the cytotoxicity of prelamin A arises in part, from it actively competing against mature lamin A to bind PCNA and that this destabilises DNA replication to induce fork stalling which in turn contributes to genomic instability.
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spelling pubmed-51206012017-06-28 Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling Cobb, Andrew M. Murray, Thomas V. Warren, Derek T. Liu, Yiwen Shanahan, Catherine M. Nucleus Research Paper The accumulation of prelamin A is linked to disruption of cellular homeostasis, tissue degeneration and aging. Its expression is implicated in compromised genome stability and increased levels of DNA damage, but to date there is no complete explanation for how prelamin A exerts its toxic effects. As the nuclear lamina is important for DNA replication we wanted to investigate the relationship between prelamin A expression and DNA replication fork stability. In this study we report that the expression of prelamin A in U2OS cells induced both mono-ubiquitination of proliferating cell nuclear antigen (PCNA) and subsequent induction of Pol η, two hallmarks of DNA replication fork stalling. Immunofluorescence microscopy revealed that cells expressing prelamin A presented with high levels of colocalisation between PCNA and γH2AX, indicating collapse of stalled DNA replication forks into DNA double-strand breaks. Subsequent protein-protein interaction assays showed prelamin A interacted with PCNA and that its presence mitigated interactions between PCNA and the mature nuclear lamina. Thus, we propose that the cytotoxicity of prelamin A arises in part, from it actively competing against mature lamin A to bind PCNA and that this destabilises DNA replication to induce fork stalling which in turn contributes to genomic instability. Taylor & Francis 2016-09-27 /pmc/articles/PMC5120601/ /pubmed/27676213 http://dx.doi.org/10.1080/19491034.2016.1239685 Text en © 2016 The Author(s). Association of American Geographers http://creativecommons.org/licenses/by/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Cobb, Andrew M.
Murray, Thomas V.
Warren, Derek T.
Liu, Yiwen
Shanahan, Catherine M.
Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title_full Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title_fullStr Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title_full_unstemmed Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title_short Disruption of PCNA-lamins A/C interactions by prelamin A induces DNA replication fork stalling
title_sort disruption of pcna-lamins a/c interactions by prelamin a induces dna replication fork stalling
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5120601/
https://www.ncbi.nlm.nih.gov/pubmed/27676213
http://dx.doi.org/10.1080/19491034.2016.1239685
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