An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation

Abstract Background Retroviruses utilize multiple unique RNA elements to control RNA processing and translation. However, it is unclear what functional RNA elements are present in endogenous retroviruses (ERVs). Gene co-option from ERVs sometimes entails the conservation of viral cis-elements requir...

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Autores principales:	Koichi Kitao, So Nakagawa, Takayuki Miyazawa
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Endogenous retroviruses RNA regulatory element Syncytin Mammalian genomes Immunologic diseases. Allergy RC581-607
Acceso en línea:	https://doaj.org/article/aa9f67d7d2b34872b681de4e7a345f48
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spelling	oai:doaj.org-article:aa9f67d7d2b34872b681de4e7a345f482021-11-14T12:38:48ZAn ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation10.1186/s12977-021-00580-21742-4690https://doaj.org/article/aa9f67d7d2b34872b681de4e7a345f482021-11-01T00:00:00Zhttps://doi.org/10.1186/s12977-021-00580-2https://doaj.org/toc/1742-4690Abstract Background Retroviruses utilize multiple unique RNA elements to control RNA processing and translation. However, it is unclear what functional RNA elements are present in endogenous retroviruses (ERVs). Gene co-option from ERVs sometimes entails the conservation of viral cis-elements required for gene expression, which might reveal the RNA regulation in ERVs. Results Here, we characterized an RNA element found in ERVs consisting of three specific sequence motifs, called SPRE. The SPRE-like elements were found in different ERV families but not in any exogenous viral sequences examined. We observed more than a thousand of copies of the SPRE-like elements in several mammalian genomes; in human and marmoset genomes, they overlapped with lineage-specific ERVs. SPRE was originally found in human syncytin-1 and syncytin-2. Indeed, several mammalian syncytin genes: mac-syncytin-3 of macaque, syncytin-Ten1 of tenrec, and syncytin-Car1 of Carnivora, contained the SPRE-like elements. A reporter assay revealed that the enhancement of gene expression by SPRE depended on the reporter genes. Mutation of SPRE impaired the wild-type syncytin-2 expression while the same mutation did not affect codon-optimized syncytin-2, suggesting that SPRE activity depends on the coding sequence. Conclusions These results indicate multiple independent invasions of various mammalian genomes by retroviruses harboring SPRE-like elements. Functional SPRE-like elements are found in several syncytin genes derived from these retroviruses. This element may facilitate the expression of viral genes, which were suppressed due to inefficient codon frequency or repressive elements within the coding sequences. These findings provide new insights into the long-term evolution of RNA elements and molecular mechanisms of gene expression in retroviruses.Koichi KitaoSo NakagawaTakayuki MiyazawaBMCarticleEndogenous retrovirusesRNA regulatory elementSyncytinMammalian genomesImmunologic diseases. AllergyRC581-607ENRetrovirology, Vol 18, Iss 1, Pp 1-15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Endogenous retroviruses RNA regulatory element Syncytin Mammalian genomes Immunologic diseases. Allergy RC581-607
spellingShingle	Endogenous retroviruses RNA regulatory element Syncytin Mammalian genomes Immunologic diseases. Allergy RC581-607 Koichi Kitao So Nakagawa Takayuki Miyazawa An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
description	Abstract Background Retroviruses utilize multiple unique RNA elements to control RNA processing and translation. However, it is unclear what functional RNA elements are present in endogenous retroviruses (ERVs). Gene co-option from ERVs sometimes entails the conservation of viral cis-elements required for gene expression, which might reveal the RNA regulation in ERVs. Results Here, we characterized an RNA element found in ERVs consisting of three specific sequence motifs, called SPRE. The SPRE-like elements were found in different ERV families but not in any exogenous viral sequences examined. We observed more than a thousand of copies of the SPRE-like elements in several mammalian genomes; in human and marmoset genomes, they overlapped with lineage-specific ERVs. SPRE was originally found in human syncytin-1 and syncytin-2. Indeed, several mammalian syncytin genes: mac-syncytin-3 of macaque, syncytin-Ten1 of tenrec, and syncytin-Car1 of Carnivora, contained the SPRE-like elements. A reporter assay revealed that the enhancement of gene expression by SPRE depended on the reporter genes. Mutation of SPRE impaired the wild-type syncytin-2 expression while the same mutation did not affect codon-optimized syncytin-2, suggesting that SPRE activity depends on the coding sequence. Conclusions These results indicate multiple independent invasions of various mammalian genomes by retroviruses harboring SPRE-like elements. Functional SPRE-like elements are found in several syncytin genes derived from these retroviruses. This element may facilitate the expression of viral genes, which were suppressed due to inefficient codon frequency or repressive elements within the coding sequences. These findings provide new insights into the long-term evolution of RNA elements and molecular mechanisms of gene expression in retroviruses.
format	article
author	Koichi Kitao So Nakagawa Takayuki Miyazawa
author_facet	Koichi Kitao So Nakagawa Takayuki Miyazawa
author_sort	Koichi Kitao
title	An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
title_short	An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
title_full	An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
title_fullStr	An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
title_full_unstemmed	An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
title_sort	ancient retroviral rna element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation
publisher	BMC
publishDate	2021
url	https://doaj.org/article/aa9f67d7d2b34872b681de4e7a345f48
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An ancient retroviral RNA element hidden in mammalian genomes and its involvement in co-opted retroviral gene regulation

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