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...
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ftczacademyscien:oai:asep.lib.cas.cz:CavUnEpca/0486275 2024-02-04T09:55:38+01:00 Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes Franke, V. Ganesh, S. (Sravya) Karlic, R. Malík, R. (Radek) Pasulka, J. (Josef) Horvat, F. Kuzman, M. Fulka, H. (Helena) Černohorská, M. (Markéta) Urbanová, J. (Jana) Svobodová, E. (Eliška) Ma, J. Suzuki, Y. Aoki, F. Schultz, R. M. Vlahovicek, K. Svoboda, P. (Petr) 2017 https://doi.org/10.1101/gr.216150.116 http://hdl.handle.net/11104/0281145 eng eng info:eu-repo/grantAgreement/EC/H2020/647403/EU//D-FENS info:eu-repo/semantics/altIdentifier/pmid/28522611 doi:10.1101/gr.216150.116 urn:pissn: 1088-9051 urn:eissn: 1549-5469 http://hdl.handle.net/11104/0281145 info:eu-repo/semantics/restrictedAccess murine endogenous retrovirus antarctic notothenioid fish embryonic stem-cells transposable elements mouse oocytes muerv-l preimplantation embryos methylation landscape regulatory networks dna methylation info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 2017 ftczacademyscien https://doi.org/10.1101/gr.216150.116 2024-01-09T17:41:34Z 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. Article in Journal/Newspaper Antarc* Antarctic The Czech Academy of Sciences: Publication Activity (ASEP) Antarctic Genome Research 27 8 1384 1394 |
institution |
Open Polar |
collection |
The Czech Academy of Sciences: Publication Activity (ASEP) |
op_collection_id |
ftczacademyscien |
language |
English |
topic |
murine endogenous retrovirus antarctic notothenioid fish embryonic stem-cells transposable elements mouse oocytes muerv-l preimplantation embryos methylation landscape regulatory networks dna methylation |
spellingShingle |
murine endogenous retrovirus antarctic notothenioid fish embryonic stem-cells transposable elements mouse oocytes muerv-l preimplantation embryos methylation landscape regulatory networks dna methylation Franke, V. Ganesh, S. (Sravya) Karlic, R. Malík, R. (Radek) Pasulka, J. (Josef) Horvat, F. Kuzman, M. Fulka, H. (Helena) Černohorská, M. (Markéta) Urbanová, J. (Jana) Svobodová, E. (Eliška) Ma, J. Suzuki, Y. Aoki, F. Schultz, R. M. Vlahovicek, K. Svoboda, P. (Petr) Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes |
topic_facet |
murine endogenous retrovirus antarctic notothenioid fish embryonic stem-cells transposable elements mouse oocytes muerv-l preimplantation embryos methylation landscape regulatory networks dna methylation |
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. |
format |
Article in Journal/Newspaper |
author |
Franke, V. Ganesh, S. (Sravya) Karlic, R. Malík, R. (Radek) Pasulka, J. (Josef) Horvat, F. Kuzman, M. Fulka, H. (Helena) Černohorská, M. (Markéta) Urbanová, J. (Jana) Svobodová, E. (Eliška) Ma, J. Suzuki, Y. Aoki, F. Schultz, R. M. Vlahovicek, K. Svoboda, P. (Petr) |
author_facet |
Franke, V. Ganesh, S. (Sravya) Karlic, R. Malík, R. (Radek) Pasulka, J. (Josef) Horvat, F. Kuzman, M. Fulka, H. (Helena) Černohorská, M. (Markéta) Urbanová, J. (Jana) Svobodová, E. (Eliška) Ma, J. Suzuki, Y. Aoki, F. Schultz, R. M. Vlahovicek, K. Svoboda, P. (Petr) |
author_sort |
Franke, V. |
title |
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_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_sort |
long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes |
publishDate |
2017 |
url |
https://doi.org/10.1101/gr.216150.116 http://hdl.handle.net/11104/0281145 |
geographic |
Antarctic |
geographic_facet |
Antarctic |
genre |
Antarc* Antarctic |
genre_facet |
Antarc* Antarctic |
op_relation |
info:eu-repo/grantAgreement/EC/H2020/647403/EU//D-FENS info:eu-repo/semantics/altIdentifier/pmid/28522611 doi:10.1101/gr.216150.116 urn:pissn: 1088-9051 urn:eissn: 1549-5469 http://hdl.handle.net/11104/0281145 |
op_rights |
info:eu-repo/semantics/restrictedAccess |
op_doi |
https://doi.org/10.1101/gr.216150.116 |
container_title |
Genome Research |
container_volume |
27 |
container_issue |
8 |
container_start_page |
1384 |
op_container_end_page |
1394 |
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1789959699204931584 |