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YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress

The survival of cells exposed to adverse environmental conditions entails various alterations in cellular function including major changes in the transcriptome as well as a radical reprogramming of protein translation. While in mammals this process has been extensively studied, stress responses in n...

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Autores principales: Guarino, Andrea Maria, Mauro, Giuseppe Di, Ruggiero, Gennaro, Geyer, Nathalie, Delicato, Antonella, Foulkes, Nicholas S., Vallone, Daniela, Calabrò, Viola
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6588705/
https://www.ncbi.nlm.nih.gov/pubmed/31227764
http://dx.doi.org/10.1038/s41598-019-45468-6
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author Guarino, Andrea Maria
Mauro, Giuseppe Di
Ruggiero, Gennaro
Geyer, Nathalie
Delicato, Antonella
Foulkes, Nicholas S.
Vallone, Daniela
Calabrò, Viola
author_facet Guarino, Andrea Maria
Mauro, Giuseppe Di
Ruggiero, Gennaro
Geyer, Nathalie
Delicato, Antonella
Foulkes, Nicholas S.
Vallone, Daniela
Calabrò, Viola
author_sort Guarino, Andrea Maria
collection PubMed
description The survival of cells exposed to adverse environmental conditions entails various alterations in cellular function including major changes in the transcriptome as well as a radical reprogramming of protein translation. While in mammals this process has been extensively studied, stress responses in non-mammalian vertebrates remain poorly understood. One of the key cellular responses to many different types of stressors is the transient generation of structures called stress granules (SGs). These represent cytoplasmic foci where untranslated mRNAs are sorted or processed for re-initiation, degradation, or packaging into mRNPs. Here, using the evolutionarily conserved Y-box binding protein 1 (YB-1) and G3BP1 as markers, we have studied the formation of stress granules in zebrafish (D. rerio) in response to different environmental stressors. We show that following heat shock, zebrafish cells, like mammalian cells, form stress granules which contain both YB-1 and G3BP1 proteins. Moreover, zfYB-1 knockdown compromises cell viability, as well as recruitment of G3BP1 into SGs, under heat shock conditions highlighting the essential role played by YB-1 in SG assembly and cell survival. However, zebrafish PAC2 cells do not assemble YB-1-positive stress granules upon oxidative stress induced by arsenite, copper or hydrogen peroxide treatment. This contrasts with the situation in human cells where SG formation is robustly induced by exposure to oxidative stressors. Thus, our findings point to fundamental differences in the mechanisms whereby mammalian and zebrafish cells respond to oxidative stress.
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spelling pubmed-65887052019-06-28 YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress Guarino, Andrea Maria Mauro, Giuseppe Di Ruggiero, Gennaro Geyer, Nathalie Delicato, Antonella Foulkes, Nicholas S. Vallone, Daniela Calabrò, Viola Sci Rep Article The survival of cells exposed to adverse environmental conditions entails various alterations in cellular function including major changes in the transcriptome as well as a radical reprogramming of protein translation. While in mammals this process has been extensively studied, stress responses in non-mammalian vertebrates remain poorly understood. One of the key cellular responses to many different types of stressors is the transient generation of structures called stress granules (SGs). These represent cytoplasmic foci where untranslated mRNAs are sorted or processed for re-initiation, degradation, or packaging into mRNPs. Here, using the evolutionarily conserved Y-box binding protein 1 (YB-1) and G3BP1 as markers, we have studied the formation of stress granules in zebrafish (D. rerio) in response to different environmental stressors. We show that following heat shock, zebrafish cells, like mammalian cells, form stress granules which contain both YB-1 and G3BP1 proteins. Moreover, zfYB-1 knockdown compromises cell viability, as well as recruitment of G3BP1 into SGs, under heat shock conditions highlighting the essential role played by YB-1 in SG assembly and cell survival. However, zebrafish PAC2 cells do not assemble YB-1-positive stress granules upon oxidative stress induced by arsenite, copper or hydrogen peroxide treatment. This contrasts with the situation in human cells where SG formation is robustly induced by exposure to oxidative stressors. Thus, our findings point to fundamental differences in the mechanisms whereby mammalian and zebrafish cells respond to oxidative stress. Nature Publishing Group UK 2019-06-21 /pmc/articles/PMC6588705/ /pubmed/31227764 http://dx.doi.org/10.1038/s41598-019-45468-6 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Guarino, Andrea Maria
Mauro, Giuseppe Di
Ruggiero, Gennaro
Geyer, Nathalie
Delicato, Antonella
Foulkes, Nicholas S.
Vallone, Daniela
Calabrò, Viola
YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title_full YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title_fullStr YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title_full_unstemmed YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title_short YB-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
title_sort yb-1 recruitment to stress granules in zebrafish cells reveals a differential adaptive response to stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6588705/
https://www.ncbi.nlm.nih.gov/pubmed/31227764
http://dx.doi.org/10.1038/s41598-019-45468-6
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