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Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes

Retrotransposons are “copy-and-paste” insertional mutagens that substantially contribute to mammalian genome content. Retrotransposons often carry long terminal repeats (LTRs) for retrovirus-like reverse transcription and integration into the genome. We report an extraordinary impact of a group of L...

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Autores principales: Franke, Vedran, Ganesh, Sravya, Karlic, Rosa, Malik, Radek, Pasulka, Josef, Horvat, Filip, Kuzman, Maja, Fulka, Helena, Cernohorska, Marketa, Urbanova, Jana, Svobodova, Eliska, Ma, Jun, Suzuki, Yutaka, Aoki, Fugaku, Schultz, Richard M., Vlahovicek, Kristian, Svoboda, Petr
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5538554/
https://www.ncbi.nlm.nih.gov/pubmed/28522611
http://dx.doi.org/10.1101/gr.216150.116
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author Franke, Vedran
Ganesh, Sravya
Karlic, Rosa
Malik, Radek
Pasulka, Josef
Horvat, Filip
Kuzman, Maja
Fulka, Helena
Cernohorska, Marketa
Urbanova, Jana
Svobodova, Eliska
Ma, Jun
Suzuki, Yutaka
Aoki, Fugaku
Schultz, Richard M.
Vlahovicek, Kristian
Svoboda, Petr
author_facet Franke, Vedran
Ganesh, Sravya
Karlic, Rosa
Malik, Radek
Pasulka, Josef
Horvat, Filip
Kuzman, Maja
Fulka, Helena
Cernohorska, Marketa
Urbanova, Jana
Svobodova, Eliska
Ma, Jun
Suzuki, Yutaka
Aoki, Fugaku
Schultz, Richard M.
Vlahovicek, Kristian
Svoboda, Petr
author_sort Franke, Vedran
collection PubMed
description Retrotransposons are “copy-and-paste” insertional mutagens that substantially contribute to mammalian genome content. Retrotransposons often carry long terminal repeats (LTRs) for retrovirus-like reverse transcription and integration into the genome. We report an extraordinary impact of a group of LTRs from the mammalian endogenous retrovirus-related ERVL retrotransposon class on gene expression in the germline and beyond. In mouse, we identified more than 800 LTRs from ORR1, MT, MT2, and MLT families, which resemble mobile gene-remodeling platforms that supply promoters and first exons. The LTR-mediated gene remodeling also extends to hamster, human, and bovine oocytes. The LTRs function in a stage-specific manner during the oocyte-to-embryo transition by activating transcription, altering protein-coding sequences, producing noncoding RNAs, and even supporting evolution of new protein-coding genes. These functions result, for example, in recycling processed pseudogenes into mRNAs or lncRNAs with regulatory roles. The functional potential of the studied LTRs is even higher, because we show that dormant LTR promoter activity can rescue loss of an essential upstream promoter. We also report a novel protein-coding gene evolution—D6Ertd527e—in which an MT LTR provided a promoter and the 5′ exon with a functional start codon while the bulk of the protein-coding sequence evolved through a CAG repeat expansion. Altogether, ERVL LTRs provide molecular mechanisms for stochastically scanning, rewiring, and recycling genetic information on an extraordinary scale. ERVL LTRs thus offer means for a comprehensive survey of the genome's expression potential, tightly intertwining with gene expression and evolution in the germline.
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spelling pubmed-55385542017-08-09 Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes Franke, Vedran Ganesh, Sravya Karlic, Rosa Malik, Radek Pasulka, Josef Horvat, Filip Kuzman, Maja Fulka, Helena Cernohorska, Marketa Urbanova, Jana Svobodova, Eliska Ma, Jun Suzuki, Yutaka Aoki, Fugaku Schultz, Richard M. Vlahovicek, Kristian Svoboda, Petr Genome Res Research Retrotransposons are “copy-and-paste” insertional mutagens that substantially contribute to mammalian genome content. Retrotransposons often carry long terminal repeats (LTRs) for retrovirus-like reverse transcription and integration into the genome. We report an extraordinary impact of a group of LTRs from the mammalian endogenous retrovirus-related ERVL retrotransposon class on gene expression in the germline and beyond. In mouse, we identified more than 800 LTRs from ORR1, MT, MT2, and MLT families, which resemble mobile gene-remodeling platforms that supply promoters and first exons. The LTR-mediated gene remodeling also extends to hamster, human, and bovine oocytes. The LTRs function in a stage-specific manner during the oocyte-to-embryo transition by activating transcription, altering protein-coding sequences, producing noncoding RNAs, and even supporting evolution of new protein-coding genes. These functions result, for example, in recycling processed pseudogenes into mRNAs or lncRNAs with regulatory roles. The functional potential of the studied LTRs is even higher, because we show that dormant LTR promoter activity can rescue loss of an essential upstream promoter. We also report a novel protein-coding gene evolution—D6Ertd527e—in which an MT LTR provided a promoter and the 5′ exon with a functional start codon while the bulk of the protein-coding sequence evolved through a CAG repeat expansion. Altogether, ERVL LTRs provide molecular mechanisms for stochastically scanning, rewiring, and recycling genetic information on an extraordinary scale. ERVL LTRs thus offer means for a comprehensive survey of the genome's expression potential, tightly intertwining with gene expression and evolution in the germline. Cold Spring Harbor Laboratory Press 2017-08 /pmc/articles/PMC5538554/ /pubmed/28522611 http://dx.doi.org/10.1101/gr.216150.116 Text en © 2017 Franke et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Franke, Vedran
Ganesh, Sravya
Karlic, Rosa
Malik, Radek
Pasulka, Josef
Horvat, Filip
Kuzman, Maja
Fulka, Helena
Cernohorska, Marketa
Urbanova, Jana
Svobodova, Eliska
Ma, Jun
Suzuki, Yutaka
Aoki, Fugaku
Schultz, Richard M.
Vlahovicek, Kristian
Svoboda, Petr
Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title_full Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title_fullStr Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title_full_unstemmed Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title_short Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
title_sort long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5538554/
https://www.ncbi.nlm.nih.gov/pubmed/28522611
http://dx.doi.org/10.1101/gr.216150.116
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