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The circular RNA Edis regulates neurodevelopment and innate immunity

Circular RNAs (circRNAs) are widely expressed in eukaryotes. However, only a subset has been functionally characterized. We identify and validate a collection of circRNAs in Drosophila, and show that depletion of the brain-enriched circRNA Edis (circ_Ect4) causes hyperactivation of antibacterial inn...

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Autores principales: Xiong, Xiao-Peng, Liang, Weihong, Liu, Wei, Xu, Shiyu, Li, Jian-Liang, Tito, Antonio, Situ, Julia, Martinez, Daniel, Wu, Chunlai, Perera, Ranjan J., Zhang, Sheng, Zhou, Rui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612488/
https://www.ncbi.nlm.nih.gov/pubmed/36301822
http://dx.doi.org/10.1371/journal.pgen.1010429
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author Xiong, Xiao-Peng
Liang, Weihong
Liu, Wei
Xu, Shiyu
Li, Jian-Liang
Tito, Antonio
Situ, Julia
Martinez, Daniel
Wu, Chunlai
Perera, Ranjan J.
Zhang, Sheng
Zhou, Rui
author_facet Xiong, Xiao-Peng
Liang, Weihong
Liu, Wei
Xu, Shiyu
Li, Jian-Liang
Tito, Antonio
Situ, Julia
Martinez, Daniel
Wu, Chunlai
Perera, Ranjan J.
Zhang, Sheng
Zhou, Rui
author_sort Xiong, Xiao-Peng
collection PubMed
description Circular RNAs (circRNAs) are widely expressed in eukaryotes. However, only a subset has been functionally characterized. We identify and validate a collection of circRNAs in Drosophila, and show that depletion of the brain-enriched circRNA Edis (circ_Ect4) causes hyperactivation of antibacterial innate immunity both in cultured cells and in vivo. Notably, Edis depleted flies display heightened resistance to bacterial infection and enhanced pathogen clearance. Conversely, ectopic Edis expression blocks innate immunity signaling. In addition, inactivation of Edis in vivo leads to impaired locomotor activity and shortened lifespan. Remarkably, these phenotypes can be recapitulated with neuron-specific depletion of Edis, accompanied by defective neurodevelopment. Furthermore, inactivation of Relish suppresses the innate immunity hyperactivation phenotype in the fly brain. Moreover, we provide evidence that Edis encodes a functional protein that associates with and compromises the processing and activation of the immune transcription factor Relish. Importantly, restoring Edis expression or ectopic expression of Edis-encoded protein suppresses both innate immunity and neurodevelopment phenotypes elicited by Edis depletion. Thus, our study establishes Edis as a key regulator of neurodevelopment and innate immunity.
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spelling pubmed-96124882022-10-28 The circular RNA Edis regulates neurodevelopment and innate immunity Xiong, Xiao-Peng Liang, Weihong Liu, Wei Xu, Shiyu Li, Jian-Liang Tito, Antonio Situ, Julia Martinez, Daniel Wu, Chunlai Perera, Ranjan J. Zhang, Sheng Zhou, Rui PLoS Genet Research Article Circular RNAs (circRNAs) are widely expressed in eukaryotes. However, only a subset has been functionally characterized. We identify and validate a collection of circRNAs in Drosophila, and show that depletion of the brain-enriched circRNA Edis (circ_Ect4) causes hyperactivation of antibacterial innate immunity both in cultured cells and in vivo. Notably, Edis depleted flies display heightened resistance to bacterial infection and enhanced pathogen clearance. Conversely, ectopic Edis expression blocks innate immunity signaling. In addition, inactivation of Edis in vivo leads to impaired locomotor activity and shortened lifespan. Remarkably, these phenotypes can be recapitulated with neuron-specific depletion of Edis, accompanied by defective neurodevelopment. Furthermore, inactivation of Relish suppresses the innate immunity hyperactivation phenotype in the fly brain. Moreover, we provide evidence that Edis encodes a functional protein that associates with and compromises the processing and activation of the immune transcription factor Relish. Importantly, restoring Edis expression or ectopic expression of Edis-encoded protein suppresses both innate immunity and neurodevelopment phenotypes elicited by Edis depletion. Thus, our study establishes Edis as a key regulator of neurodevelopment and innate immunity. Public Library of Science 2022-10-27 /pmc/articles/PMC9612488/ /pubmed/36301822 http://dx.doi.org/10.1371/journal.pgen.1010429 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Xiong, Xiao-Peng
Liang, Weihong
Liu, Wei
Xu, Shiyu
Li, Jian-Liang
Tito, Antonio
Situ, Julia
Martinez, Daniel
Wu, Chunlai
Perera, Ranjan J.
Zhang, Sheng
Zhou, Rui
The circular RNA Edis regulates neurodevelopment and innate immunity
title The circular RNA Edis regulates neurodevelopment and innate immunity
title_full The circular RNA Edis regulates neurodevelopment and innate immunity
title_fullStr The circular RNA Edis regulates neurodevelopment and innate immunity
title_full_unstemmed The circular RNA Edis regulates neurodevelopment and innate immunity
title_short The circular RNA Edis regulates neurodevelopment and innate immunity
title_sort circular rna edis regulates neurodevelopment and innate immunity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612488/
https://www.ncbi.nlm.nih.gov/pubmed/36301822
http://dx.doi.org/10.1371/journal.pgen.1010429
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