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Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline

BACKGROUND: The 3′ untranslated regions (UTRs) of mRNAs play a major role in post-transcriptional regulation of gene expression. Selection of transcript cleavage and polyadenylation sites is a dynamic process that produces multiple transcript isoforms for the same gene within and across different ce...

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Autores principales: West, Sean M., Mecenas, Desirea, Gutwein, Michelle, Aristizábal-Corrales, David, Piano, Fabio, Gunsalus, Kristin C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5784609/
https://www.ncbi.nlm.nih.gov/pubmed/29368663
http://dx.doi.org/10.1186/s13059-017-1369-x
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author West, Sean M.
Mecenas, Desirea
Gutwein, Michelle
Aristizábal-Corrales, David
Piano, Fabio
Gunsalus, Kristin C.
author_facet West, Sean M.
Mecenas, Desirea
Gutwein, Michelle
Aristizábal-Corrales, David
Piano, Fabio
Gunsalus, Kristin C.
author_sort West, Sean M.
collection PubMed
description BACKGROUND: The 3′ untranslated regions (UTRs) of mRNAs play a major role in post-transcriptional regulation of gene expression. Selection of transcript cleavage and polyadenylation sites is a dynamic process that produces multiple transcript isoforms for the same gene within and across different cell types. Using LITE-Seq, a new quantitative method to capture transcript 3′ ends expressed in vivo, we have characterized sex- and cell type-specific transcriptome-wide changes in gene expression and 3′UTR diversity in Caenorhabditis elegans germline cells undergoing proliferation and differentiation. RESULTS: We show that nearly half of germline transcripts are alternatively polyadenylated, that differential regulation of endogenous 3′UTR variants is common, and that alternative isoforms direct distinct spatiotemporal protein expression patterns in vivo. Dynamic expression profiling also reveals temporal regulation of X-linked gene expression, selective stabilization of transcripts, and strong evidence for a novel developmental program that promotes nucleolar dissolution in oocytes. We show that the RNA-binding protein NCL-1/Brat is a posttranscriptional regulator of numerous ribosome-related transcripts that acts through specific U-rich binding motifs to down-regulate mRNAs encoding ribosomal protein subunits, rRNA processing factors, and tRNA synthetases. CONCLUSIONS: These results highlight the pervasive nature and functional potential of patterned gene and isoform expression during early animal development.
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spelling pubmed-57846092018-02-07 Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline West, Sean M. Mecenas, Desirea Gutwein, Michelle Aristizábal-Corrales, David Piano, Fabio Gunsalus, Kristin C. Genome Biol Research BACKGROUND: The 3′ untranslated regions (UTRs) of mRNAs play a major role in post-transcriptional regulation of gene expression. Selection of transcript cleavage and polyadenylation sites is a dynamic process that produces multiple transcript isoforms for the same gene within and across different cell types. Using LITE-Seq, a new quantitative method to capture transcript 3′ ends expressed in vivo, we have characterized sex- and cell type-specific transcriptome-wide changes in gene expression and 3′UTR diversity in Caenorhabditis elegans germline cells undergoing proliferation and differentiation. RESULTS: We show that nearly half of germline transcripts are alternatively polyadenylated, that differential regulation of endogenous 3′UTR variants is common, and that alternative isoforms direct distinct spatiotemporal protein expression patterns in vivo. Dynamic expression profiling also reveals temporal regulation of X-linked gene expression, selective stabilization of transcripts, and strong evidence for a novel developmental program that promotes nucleolar dissolution in oocytes. We show that the RNA-binding protein NCL-1/Brat is a posttranscriptional regulator of numerous ribosome-related transcripts that acts through specific U-rich binding motifs to down-regulate mRNAs encoding ribosomal protein subunits, rRNA processing factors, and tRNA synthetases. CONCLUSIONS: These results highlight the pervasive nature and functional potential of patterned gene and isoform expression during early animal development. BioMed Central 2018-01-24 /pmc/articles/PMC5784609/ /pubmed/29368663 http://dx.doi.org/10.1186/s13059-017-1369-x Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
West, Sean M.
Mecenas, Desirea
Gutwein, Michelle
Aristizábal-Corrales, David
Piano, Fabio
Gunsalus, Kristin C.
Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title_full Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title_fullStr Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title_full_unstemmed Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title_short Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline
title_sort developmental dynamics of gene expression and alternative polyadenylation in the caenorhabditis elegans germline
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5784609/
https://www.ncbi.nlm.nih.gov/pubmed/29368663
http://dx.doi.org/10.1186/s13059-017-1369-x
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