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Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells

BACKGROUND: Bats are a major reservoir of zoonotic viruses, and there has been growing interest in characterizing bat-specific features of innate immunity and inflammation. Recent studies have revealed bat-specific adaptations affecting interferon (IFN) signaling and IFN-stimulated genes (ISGs), but...

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Autores principales: Pasquesi, Giulia Irene Maria, Kelly, Conor J., Ordonez, Andrea D., Chuong, Edward B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446614/
https://www.ncbi.nlm.nih.gov/pubmed/36068622
http://dx.doi.org/10.1186/s13100-022-00277-z
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author Pasquesi, Giulia Irene Maria
Kelly, Conor J.
Ordonez, Andrea D.
Chuong, Edward B.
author_facet Pasquesi, Giulia Irene Maria
Kelly, Conor J.
Ordonez, Andrea D.
Chuong, Edward B.
author_sort Pasquesi, Giulia Irene Maria
collection PubMed
description BACKGROUND: Bats are a major reservoir of zoonotic viruses, and there has been growing interest in characterizing bat-specific features of innate immunity and inflammation. Recent studies have revealed bat-specific adaptations affecting interferon (IFN) signaling and IFN-stimulated genes (ISGs), but we still have a limited understanding of the genetic mechanisms that have shaped the evolution of bat immunity. Here we investigated the transcriptional and epigenetic dynamics of transposable elements (TEs) during the type I IFN response in little brown bat (Myotis lucifugus) primary embryonic fibroblast cells, using RNA-seq and CUT&RUN. RESULTS: We found multiple bat-specific TEs that undergo both locus-specific and family-level transcriptional induction in response to IFN. Our transcriptome reassembly identified multiple ISGs that have acquired novel exons from bat-specific TEs, including NLRC5, SLNF5 and a previously unannotated isoform of the IFITM2 gene. We also identified examples of TE-derived regulatory elements, but did not find strong evidence supporting genome-wide epigenetic activation of TEs in response to IFN. CONCLUSION: Collectively, our study uncovers numerous TE-derived transcripts, proteins, and alternative isoforms that are induced by IFN in Myotis lucifugus cells, highlighting candidate loci that may contribute to bat-specific immune function. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13100-022-00277-z.
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spelling pubmed-94466142022-09-06 Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells Pasquesi, Giulia Irene Maria Kelly, Conor J. Ordonez, Andrea D. Chuong, Edward B. Mob DNA Research BACKGROUND: Bats are a major reservoir of zoonotic viruses, and there has been growing interest in characterizing bat-specific features of innate immunity and inflammation. Recent studies have revealed bat-specific adaptations affecting interferon (IFN) signaling and IFN-stimulated genes (ISGs), but we still have a limited understanding of the genetic mechanisms that have shaped the evolution of bat immunity. Here we investigated the transcriptional and epigenetic dynamics of transposable elements (TEs) during the type I IFN response in little brown bat (Myotis lucifugus) primary embryonic fibroblast cells, using RNA-seq and CUT&RUN. RESULTS: We found multiple bat-specific TEs that undergo both locus-specific and family-level transcriptional induction in response to IFN. Our transcriptome reassembly identified multiple ISGs that have acquired novel exons from bat-specific TEs, including NLRC5, SLNF5 and a previously unannotated isoform of the IFITM2 gene. We also identified examples of TE-derived regulatory elements, but did not find strong evidence supporting genome-wide epigenetic activation of TEs in response to IFN. CONCLUSION: Collectively, our study uncovers numerous TE-derived transcripts, proteins, and alternative isoforms that are induced by IFN in Myotis lucifugus cells, highlighting candidate loci that may contribute to bat-specific immune function. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13100-022-00277-z. BioMed Central 2022-09-06 /pmc/articles/PMC9446614/ /pubmed/36068622 http://dx.doi.org/10.1186/s13100-022-00277-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Pasquesi, Giulia Irene Maria
Kelly, Conor J.
Ordonez, Andrea D.
Chuong, Edward B.
Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title_full Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title_fullStr Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title_full_unstemmed Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title_short Transcriptional dynamics of transposable elements in the type I IFN response in Myotis lucifugus cells
title_sort transcriptional dynamics of transposable elements in the type i ifn response in myotis lucifugus cells
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446614/
https://www.ncbi.nlm.nih.gov/pubmed/36068622
http://dx.doi.org/10.1186/s13100-022-00277-z
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