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Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development

Animal development requires the execution of specific transcriptional programs in different sets of cells to build tissues and functional organs. Transcripts are exported from the nucleus to the cytoplasm where they are translated into proteins that, ultimately, carry out the cellular functions. Her...

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Autores principales: Zheleva, Angelina, Gómez-Orte, Eva, Sáenz-Narciso, Beatriz, Ezcurra, Begoña, Kassahun, Henok, de Toro, María, Miranda-Vizuete, Antonio, Schnabel, Ralf, Nilsen, Hilde, Cabello, Juan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6762213/
https://www.ncbi.nlm.nih.gov/pubmed/31525188
http://dx.doi.org/10.1371/journal.pgen.1008338
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author Zheleva, Angelina
Gómez-Orte, Eva
Sáenz-Narciso, Beatriz
Ezcurra, Begoña
Kassahun, Henok
de Toro, María
Miranda-Vizuete, Antonio
Schnabel, Ralf
Nilsen, Hilde
Cabello, Juan
author_facet Zheleva, Angelina
Gómez-Orte, Eva
Sáenz-Narciso, Beatriz
Ezcurra, Begoña
Kassahun, Henok
de Toro, María
Miranda-Vizuete, Antonio
Schnabel, Ralf
Nilsen, Hilde
Cabello, Juan
author_sort Zheleva, Angelina
collection PubMed
description Animal development requires the execution of specific transcriptional programs in different sets of cells to build tissues and functional organs. Transcripts are exported from the nucleus to the cytoplasm where they are translated into proteins that, ultimately, carry out the cellular functions. Here we show that in Caenorhabditis elegans, reduction of mRNA export strongly affects epithelial morphogenesis and germline proliferation while other tissues remain relatively unaffected. Epithelialization and gamete formation demand a large number of transcripts in the cytoplasm for the duration of these processes. In addition, our findings highlight the existence of a regulatory feedback mechanism that activates gene expression in response to low levels of cytoplasmic mRNA. We expand the genetic characterization of nuclear export factor NXF-1 to other members of the mRNA export pathway to model mRNA export and recycling of NXF-1 back to the nucleus. Our model explains how mutations in genes involved in general processes, such as mRNA export, may result in tissue-specific developmental phenotypes.
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spelling pubmed-67622132019-10-11 Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development Zheleva, Angelina Gómez-Orte, Eva Sáenz-Narciso, Beatriz Ezcurra, Begoña Kassahun, Henok de Toro, María Miranda-Vizuete, Antonio Schnabel, Ralf Nilsen, Hilde Cabello, Juan PLoS Genet Research Article Animal development requires the execution of specific transcriptional programs in different sets of cells to build tissues and functional organs. Transcripts are exported from the nucleus to the cytoplasm where they are translated into proteins that, ultimately, carry out the cellular functions. Here we show that in Caenorhabditis elegans, reduction of mRNA export strongly affects epithelial morphogenesis and germline proliferation while other tissues remain relatively unaffected. Epithelialization and gamete formation demand a large number of transcripts in the cytoplasm for the duration of these processes. In addition, our findings highlight the existence of a regulatory feedback mechanism that activates gene expression in response to low levels of cytoplasmic mRNA. We expand the genetic characterization of nuclear export factor NXF-1 to other members of the mRNA export pathway to model mRNA export and recycling of NXF-1 back to the nucleus. Our model explains how mutations in genes involved in general processes, such as mRNA export, may result in tissue-specific developmental phenotypes. Public Library of Science 2019-09-16 /pmc/articles/PMC6762213/ /pubmed/31525188 http://dx.doi.org/10.1371/journal.pgen.1008338 Text en © 2019 Zheleva et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Zheleva, Angelina
Gómez-Orte, Eva
Sáenz-Narciso, Beatriz
Ezcurra, Begoña
Kassahun, Henok
de Toro, María
Miranda-Vizuete, Antonio
Schnabel, Ralf
Nilsen, Hilde
Cabello, Juan
Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title_full Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title_fullStr Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title_full_unstemmed Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title_short Reduction of mRNA export unmasks different tissue sensitivities to low mRNA levels during Caenorhabditis elegans development
title_sort reduction of mrna export unmasks different tissue sensitivities to low mrna levels during caenorhabditis elegans development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6762213/
https://www.ncbi.nlm.nih.gov/pubmed/31525188
http://dx.doi.org/10.1371/journal.pgen.1008338
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