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Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect

Autophagy plays an important role in virus infection of the host, because viral components and particles can be degraded by the host’s autophagy and some viruses may be able to hijack and subvert autophagy for its benefit. However, details on the mechanisms that govern autophagy for immunity against...

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Autores principales: Zhang, Lu, Liu, Wenwen, Wu, Nan, Wang, Hui, Zhang, Zhongkai, Liu, Yule, Wang, Xifeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907856/
https://www.ncbi.nlm.nih.gov/pubmed/36706154
http://dx.doi.org/10.1371/journal.ppat.1011134
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author Zhang, Lu
Liu, Wenwen
Wu, Nan
Wang, Hui
Zhang, Zhongkai
Liu, Yule
Wang, Xifeng
author_facet Zhang, Lu
Liu, Wenwen
Wu, Nan
Wang, Hui
Zhang, Zhongkai
Liu, Yule
Wang, Xifeng
author_sort Zhang, Lu
collection PubMed
description Autophagy plays an important role in virus infection of the host, because viral components and particles can be degraded by the host’s autophagy and some viruses may be able to hijack and subvert autophagy for its benefit. However, details on the mechanisms that govern autophagy for immunity against viral infections or benefit viral survival remain largely unknown. Plant reoviruses such as southern rice black-streaked dwarf virus (SRBSDV), which seriously threaten crop yield, are only transmitted by vector insects. Here, we report a novel mechanism by which SRBSDV induces incomplete autophagy by blocking autophagosome-lysosome fusion, resulting in viral accumulation in gut epithelial cells of its vector, white-backed planthopper (Sogatella furcifera). SRBSDV infection leads to stimulation of the c-Jun N-terminal kinase (JNK) signaling pathway, which further activates autophagy. Mature and assembling virions were found close to the edge7 of the outer membrane of autophagosomes. Inhibition autophagy leads to the decrease of autophagosomes, which resulting in impaired maturation of virions and the decrease of virus titer, whereas activation of autophagy facilitated virus titer. Further, SRBSDV inhibited fusion of autophagosomes and lysosomes by interacting with lysosomal-associated membrane protein 1 (LAMP1) using viral P10. Thus, SRBSDV not only avoids being degrading by lysosomes, but also further hijacks these non-fusing autophagosomes for its subsistence. Our findings reveal a novel mechanism of reovirus persistence, which can explain why SRBSDV can be acquired and transmitted rapidly by its insect vector.
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spelling pubmed-99078562023-02-08 Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect Zhang, Lu Liu, Wenwen Wu, Nan Wang, Hui Zhang, Zhongkai Liu, Yule Wang, Xifeng PLoS Pathog Research Article Autophagy plays an important role in virus infection of the host, because viral components and particles can be degraded by the host’s autophagy and some viruses may be able to hijack and subvert autophagy for its benefit. However, details on the mechanisms that govern autophagy for immunity against viral infections or benefit viral survival remain largely unknown. Plant reoviruses such as southern rice black-streaked dwarf virus (SRBSDV), which seriously threaten crop yield, are only transmitted by vector insects. Here, we report a novel mechanism by which SRBSDV induces incomplete autophagy by blocking autophagosome-lysosome fusion, resulting in viral accumulation in gut epithelial cells of its vector, white-backed planthopper (Sogatella furcifera). SRBSDV infection leads to stimulation of the c-Jun N-terminal kinase (JNK) signaling pathway, which further activates autophagy. Mature and assembling virions were found close to the edge7 of the outer membrane of autophagosomes. Inhibition autophagy leads to the decrease of autophagosomes, which resulting in impaired maturation of virions and the decrease of virus titer, whereas activation of autophagy facilitated virus titer. Further, SRBSDV inhibited fusion of autophagosomes and lysosomes by interacting with lysosomal-associated membrane protein 1 (LAMP1) using viral P10. Thus, SRBSDV not only avoids being degrading by lysosomes, but also further hijacks these non-fusing autophagosomes for its subsistence. Our findings reveal a novel mechanism of reovirus persistence, which can explain why SRBSDV can be acquired and transmitted rapidly by its insect vector. Public Library of Science 2023-01-27 /pmc/articles/PMC9907856/ /pubmed/36706154 http://dx.doi.org/10.1371/journal.ppat.1011134 Text en © 2023 Zhang et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Zhang, Lu
Liu, Wenwen
Wu, Nan
Wang, Hui
Zhang, Zhongkai
Liu, Yule
Wang, Xifeng
Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title_full Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title_fullStr Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title_full_unstemmed Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title_short Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
title_sort southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907856/
https://www.ncbi.nlm.nih.gov/pubmed/36706154
http://dx.doi.org/10.1371/journal.ppat.1011134
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