Extracellular vesicles originating from autophagy mediate an antibody-resistant spread of classical swine fever virus in cell culture

Wang, Tao; Zhang, Liang; Liang, Wan; Liu, Shanchuan; Deng, Wen; Liu, Yangruiyu; Liu, Yaru; Song, Mengzhao; Guo, Kangkang; Zhang, Yanming

doi:10.1080/15548627.2021.1987673

Cited by 14 publications

(8 citation statements)

References 55 publications

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“…CSFV can regulate autophagy through AKT-mTOR, MAPK-ERK, and CAMKK2-CaMKKβ pathways and then regulate cell apoptosis and maintain virus replication [ 32 ]. CSFV can be enriched into autophagic double vesicles for reproduction secreted out of the cell through autophagic vesicles and then evasion the recognition of neutralizing antibodies, which is conducive to cell-to-cell transmission [ 22 , 33 ].…”

Section: Discussionmentioning

confidence: 99%

The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection

Song

Zhao

et al. 2023

Emerging Microbes & Infections

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CSFV (classical swine fever virus) is currently endemic in developing countries in Asia and has recently re-emerged in Japan. Under the pressure of natural selection pressure, CSFV keeps evolving to maintain its ecological niche in nature. CSFV has evolved mechanisms that induce immune depression, but its pathogenic mechanism is still unclear. In this study, using transcriptomics and metabolomics methods, we found that CSFV infection alters innate host immunity by activating the interferon pathway, inhibiting host inflammation, apoptosis, and remodelling host metabolism in porcine alveolar macrophages. Moreover, we revealed that autophagy could alter innate immunity and metabolism induced by CSFV infection. Enhanced autophagy further inhibited CSFV-induced RIG-I-IRF3 signal transduction axis and JAK-STAT signalling pathway and blocked type I interferon production while reducing autophagy inhibition of the NF-κB signalling pathway and apoptosis in CSFV infection cells. Furthermore, the level of CSFV infection-induced glycolysis and the content of lactate and pyruvate, as well as 3-phosphoglyceraldehyde, a derivative of glycolysis converted to serine, was altered by autophagy. We also found that silencing HK2 (hexokinase 2), the rate-limiting enzyme of glycolytic metabolism, could induce autophagy but reduce the interferon signalling pathway, NF-κB signalling pathway, and inhibition of apoptosis induced by CSFV infection. In addition, inhibited cellular autophagy by silencing ATG5 or using 3-Methyladenine, could backfill the inhibitory effect of silencing HK2 on the cellular interferon signalling pathway, NF-κB signalling pathway, and apoptosis.

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Section: Discussionmentioning

confidence: 99%

The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection

Song

Zhao

et al. 2023

Emerging Microbes & Infections

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“…It is generally assumed that virions that assemble in the ER are exported via the COPII-mediated early secretory pathway; the virions first reach the Golgi apparatus and TGN, followed by transport to the plasma membrane and egress [ 8 ]. However, a few studies reported that the beta-coronavirus MHV use lysosomes for egress and that the enteroviruses (poliovirus) and classical swine fever virus (CSFV) release occurred via autophagy pathway [ 10 , 51 , 52 ]. Whether PEDV viral particles in COPII-coated vesicles may use the biosynthetic secretory pathway or autophagosomes/lysosomes to egress requires further investigation.…”

Section: Discussionmentioning

confidence: 99%

HDAC-Specific Inhibitors Induce the Release of Porcine Epidemic Diarrhea Virus via the COPII-Coated Vesicles

Yang,

Chen,

Zhang

et al. 2023

Viruses

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Porcine epidemic diarrhea virus (PEDV) is an alpha-coronavirus causing acute diarrhea and high mortality in neonatal suckling piglets, resulting in huge economic losses for the global swine industry. The replication, assembly and cell egression of PEDV, an enveloped RNA virus, are mediated via altered intracellular trafficking. The underlying mechanisms of PEDV secretion are poorly understood. In this study, we found that the histone deacetylase (HDAC)-specific inhibitors, trichostatin A (TSA) and sodium butyrate (NaB), facilitate the secretion of infectious PEDV particles without interfering with its assembly. We found that PEDV N protein and its replicative intermediate dsRNA colocalize with coat protein complex II (COPII)-coated vesicles. We also showed that the colocalization of PEDV and COPII is enhanced by the HDAC-specific inhibitors. In addition, ultrastructural analysis revealed that the HDAC-specific inhibitors promote COPII-coated vesicles carrying PEDV virions and the secretion of COPII-coated vesicles. Consistently, HDAC-specific inhibitors-induced PEDV particle secretion was abolished by Sec24B knockdown, implying that the HDAC-specific inhibitors-mediated COPII-coated vesicles are required for PEDV secretion. Taken together, our findings provide initial evidence suggesting that PEDV virions can assemble in the endoplasmic reticulum (ER) and bud off from the ER in the COPII-coated vesicles. HDAC-specific inhibitors promote PEDV release by hijacking the COPII-coated vesicles.

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“…In our opinion, this problem could be clarified to some extent from the perspective of exosomes during host-virus interactions. In vertebrates, all relevant researches have shown that virus could exploit exosomes to transmit viral particles or full-length genomic RNA and help to escape the host's immune surveillance 30,34,49 . While in invertebrates, results including this study indicate that host cells could drive exosomes to present viral substances, and further activate the immune state of surrounding exosome recipient cells to resist virus invasion 25 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Exosome-mediated viral nucleic acid presentation in a crustacean reveals innate immunity evolution from a novel perspective

Gong

Zhao

et al. 2022

Preprint

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As an enduring hot topic in the field of innate immunity, apoptosis is widely considered as an effective approach to eliminate pathogenic microbes, and possesses crucial role during host-pathogen interactions. Recently, researchers have found that virus-containing host cells could transmit apoptotic signals to surrounding uninfected cells during infection, but the mechanism remains unclear. Here, we found that exosomes secreted by WSSV-infected mud crab hemocytes contain viral nucleic acid wsv277, which could be transported to the recipient cells and further expressed viral protein with phosphokinase activity. Besides, by using transcriptome, proteome, ChIP-seq and coIP techniques, the results revealed that wsv277 could activate the transcription and translation of apoptotic genes via interacting with CBF and EF-1α, so as to suppress the spread of virus infection by inducing apoptosis of the surrounding cells. Therefore, for the first time, our study proved that the components of DNA virus could be encapsulated into exosomes, and elucidated the mechanism of apoptotic signal transduction between cells from the perspective of exosome. Moreover, comparing those of invertebrates, we hypothesized that the innate immune system of vertebrate was weakened or degenerated, allowing exosomes to be employed by virus as the vehicle for immune escape.

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Extracellular vesicles originating from autophagy mediate an antibody-resistant spread of classical swine fever virus in cell culture

Cited by 14 publications

References 55 publications

The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection

The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection

HDAC-Specific Inhibitors Induce the Release of Porcine Epidemic Diarrhea Virus via the COPII-Coated Vesicles

Exosome-mediated viral nucleic acid presentation in a crustacean reveals innate immunity evolution from a novel perspective

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