Cargando…

Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression

In response to adverse environmental cues, Caenorhabditis elegans larvae can temporarily arrest development at the second moult and form dauers, a diapause stage that allows for long-term survival. This process is largely regulated by certain evolutionarily conserved signal transduction pathways, bu...

Descripción completa

Detalles Bibliográficos
Autores principales: Borbolis, Fivos, Flessa, Christina-Maria, Roumelioti, Fani, Diallinas, George, Stravopodis, Dimitrios J., Syntichaki, Popi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5376704/
https://www.ncbi.nlm.nih.gov/pubmed/28250105
http://dx.doi.org/10.1098/rsob.160313
_version_ 1782519203349135360
author Borbolis, Fivos
Flessa, Christina-Maria
Roumelioti, Fani
Diallinas, George
Stravopodis, Dimitrios J.
Syntichaki, Popi
author_facet Borbolis, Fivos
Flessa, Christina-Maria
Roumelioti, Fani
Diallinas, George
Stravopodis, Dimitrios J.
Syntichaki, Popi
author_sort Borbolis, Fivos
collection PubMed
description In response to adverse environmental cues, Caenorhabditis elegans larvae can temporarily arrest development at the second moult and form dauers, a diapause stage that allows for long-term survival. This process is largely regulated by certain evolutionarily conserved signal transduction pathways, but it is also affected by miRNA-mediated post-transcriptional control of gene expression. The 5′–3′ mRNA decay mechanism contributes to miRNA-mediated silencing of target mRNAs in many organisms but how it affects developmental decisions during normal or stress conditions is largely unknown. Here, we show that loss of the mRNA decapping complex activity acting in the 5′–3′ mRNA decay pathway inhibits dauer formation at the stressful high temperature of 27.5°C, and instead promotes early developmental arrest. Our genetic data suggest that this arrest phenotype correlates with dysregulation of heterochronic gene expression and an aberrant stabilization of lin-14 mRNA at early larval stages. Restoration of neuronal dcap-1 activity was sufficient to rescue growth phenotypes of dcap-1 mutants at both high and normal temperatures, implying the involvement of common developmental timing mechanisms. Our work unveils the crucial role of 5′–3′ mRNA degradation in proper regulation of heterochronic gene expression programmes, which proved to be essential for survival under stressful conditions.
format Online
Article
Text
id pubmed-5376704
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher The Royal Society
record_format MEDLINE/PubMed
spelling pubmed-53767042017-04-06 Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression Borbolis, Fivos Flessa, Christina-Maria Roumelioti, Fani Diallinas, George Stravopodis, Dimitrios J. Syntichaki, Popi Open Biol Research In response to adverse environmental cues, Caenorhabditis elegans larvae can temporarily arrest development at the second moult and form dauers, a diapause stage that allows for long-term survival. This process is largely regulated by certain evolutionarily conserved signal transduction pathways, but it is also affected by miRNA-mediated post-transcriptional control of gene expression. The 5′–3′ mRNA decay mechanism contributes to miRNA-mediated silencing of target mRNAs in many organisms but how it affects developmental decisions during normal or stress conditions is largely unknown. Here, we show that loss of the mRNA decapping complex activity acting in the 5′–3′ mRNA decay pathway inhibits dauer formation at the stressful high temperature of 27.5°C, and instead promotes early developmental arrest. Our genetic data suggest that this arrest phenotype correlates with dysregulation of heterochronic gene expression and an aberrant stabilization of lin-14 mRNA at early larval stages. Restoration of neuronal dcap-1 activity was sufficient to rescue growth phenotypes of dcap-1 mutants at both high and normal temperatures, implying the involvement of common developmental timing mechanisms. Our work unveils the crucial role of 5′–3′ mRNA degradation in proper regulation of heterochronic gene expression programmes, which proved to be essential for survival under stressful conditions. The Royal Society 2017-03-01 /pmc/articles/PMC5376704/ /pubmed/28250105 http://dx.doi.org/10.1098/rsob.160313 Text en © 2017 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Borbolis, Fivos
Flessa, Christina-Maria
Roumelioti, Fani
Diallinas, George
Stravopodis, Dimitrios J.
Syntichaki, Popi
Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title_full Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title_fullStr Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title_full_unstemmed Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title_short Neuronal function of the mRNA decapping complex determines survival of Caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
title_sort neuronal function of the mrna decapping complex determines survival of caenorhabditis elegans at high temperature through temporal regulation of heterochronic gene expression
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5376704/
https://www.ncbi.nlm.nih.gov/pubmed/28250105
http://dx.doi.org/10.1098/rsob.160313
work_keys_str_mv AT borbolisfivos neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression
AT flessachristinamaria neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression
AT roumeliotifani neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression
AT diallinasgeorge neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression
AT stravopodisdimitriosj neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression
AT syntichakipopi neuronalfunctionofthemrnadecappingcomplexdeterminessurvivalofcaenorhabditiselegansathightemperaturethroughtemporalregulationofheterochronicgeneexpression