A nonstructural protein encoded by a rice reovirus induces an incomplete autophagy to promote viral spread in insect vectors

Viruses can hijack autophagosomes as the nonlytic release vehicles in cultured host cells. However, how autophagosome-mediated viral spread occurs in infected host tissues or organs in vivo remains poorly understood. Here, we report that an important rice reovirus, rice gall dwarf virus (RGDV) hijac...

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Published in:PLoS pathogens Vol. 18; no. 5; p. e1010506
Main Authors: Jia, Dongsheng, Liang, Qifu, Liu, Huan, Li, Guangjun, Zhang, Xiaofeng, Chen, Qian, Wang, Aiming, Wei, Taiyun
Format: Journal Article
Language:English
Published: United States Public Library of Science 01.05.2022
Public Library of Science (PLoS)
Subjects:
Antibodies
Autophagy
Autophagy (Cytology)
Biology and Life Sciences
Cell death
Conjugation
Degradation
Diseases and pests
Genetic aspects
Infections
Insects
Medicine and Health Sciences
Membranes
Microscopy
Midgut
Organs
Pathogens
Phagocytosis
Phagosomes
Propagation
Properties
Proteins
Reoviruses
Research and Analysis Methods
Rice
Salivary gland
Salivary glands
Vectors
Viral infections
Viral proteins
Virulence (Microbiology)
Viruses
Taiwan
ISSN:1553-7374, 1553-7366, 1553-7374
Online Access:Get full text
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Summary:Viruses can hijack autophagosomes as the nonlytic release vehicles in cultured host cells. However, how autophagosome-mediated viral spread occurs in infected host tissues or organs in vivo remains poorly understood. Here, we report that an important rice reovirus, rice gall dwarf virus (RGDV) hijacks autophagosomes to traverse multiple insect membrane barriers in the midgut and salivary gland of leafhopper vector to enhance viral spread. Such virus-containing double-membraned autophagosomes are prevented from degradation, resulting in increased viral propagation. Mechanistically, viral nonstructural protein Pns11 induces autophagy and embeds itself in the autophagosome membranes. The autophagy-related protein 5 (ATG5)-ATG12 conjugation is essential for initial autophagosome membrane biogenesis. RGDV Pns11 specifically interacts with ATG5, both in vitro and in vivo . Silencing of ATG5 or Pns11 expression suppresses ATG8 lipidation, autophagosome formation, and efficient viral propagation. Thus, Pns11 could directly recruit ATG5-ATG12 conjugation to induce the formation of autophagosomes, facilitating viral spread within the insect bodies. Furthermore, Pns11 potentially blocks autophagosome degradation by directly targeting and mediating the reduced expression of N-glycosylated Lamp1 on lysosomal membranes. Taken together, these results highlight how RGDV remodels autophagosomes to benefit viral propagation in its insect vector.
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The authors have declared that no competing interests exist.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1010506