Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro

Peste des petits ruminants (PPR) is an acute and highly contagious disease in small ruminants that causes significant economic losses in developing countries. An increasing number of studies have demonstrated that both autophagy and apoptosis are important cellular mechanisms for maintaining homeost...

Full description

Bibliographic Details
Main Authors: Bo Yang, Qinghong Xue, Xuefeng Qi, Xueping Wang, Peilong Jia, Shuying Chen, Ting Wang, Tianxia Xue, Jingyu Wang
Format: Article
Language:English
Published: Taylor & Francis Group 2018-12-01
Series:Virulence
Subjects:
Online Access:http://dx.doi.org/10.1080/21505594.2018.1496776
_version_ 1811260948214710272
author Bo Yang
Qinghong Xue
Xuefeng Qi
Xueping Wang
Peilong Jia
Shuying Chen
Ting Wang
Tianxia Xue
Jingyu Wang
author_facet Bo Yang
Qinghong Xue
Xuefeng Qi
Xueping Wang
Peilong Jia
Shuying Chen
Ting Wang
Tianxia Xue
Jingyu Wang
author_sort Bo Yang
collection DOAJ
description Peste des petits ruminants (PPR) is an acute and highly contagious disease in small ruminants that causes significant economic losses in developing countries. An increasing number of studies have demonstrated that both autophagy and apoptosis are important cellular mechanisms for maintaining homeostasis, and they participate in the host response to pathogens. However, the crosstalk between apoptosis and autophagy in host cells during PPRV infection has not been clarified. In this study, autophagy was induced upon virus infection in caprine endometrial epithelial cells (EECs), as determined by the appearance of double- and single-membrane autophagy-like vesicles, LC3-I/LC3-II conversion, and p62 degradation. We also found that PPRV infection triggered a complete autophagic response, most likely mediated by the non-structural protein C and nucleoprotein N. Moreover, our results suggest that autophagy not only promotes the replication of PPRV in EECs but also provides a potential mechanism for inhibiting PPRV-induced apoptosis. Inhibiting autophagosome formation by wortmannin and knocking down the essential autophagic proteins Beclin-1 and ATG7 induces caspase-dependent apoptosis in EECs in PPRV infection. However, inhibiting autophagosome and lysosome fusion by NH4Cl and chloroquine did not increase the number of apoptotic cells. Collectively, these data are the first to indicate that PPRV-induced autophagy inhibits caspase-dependent apoptosis and thus contributes to the enhancement of viral replication and maturity in host cells.
first_indexed 2024-04-12T18:55:12Z
format Article
id doaj.art-de1cdf5815b542458a97f3955ace0f6c
institution Directory Open Access Journal
issn 2150-5594
2150-5608
language English
last_indexed 2024-04-12T18:55:12Z
publishDate 2018-12-01
publisher Taylor & Francis Group
record_format Article
series Virulence
spelling doaj.art-de1cdf5815b542458a97f3955ace0f6c2022-12-22T03:20:22ZengTaylor & Francis GroupVirulence2150-55942150-56082018-12-01911176119410.1080/21505594.2018.14967761496776Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitroBo Yang0Qinghong Xue1Xuefeng Qi2Xueping Wang3Peilong Jia4Shuying Chen5Ting Wang6Tianxia Xue7Jingyu Wang8Northwest A&F UniversityChina Institute of Veterinary Drug ControlNorthwest A&F UniversityNorthwest A&F UniversityNorthwest A&F UniversityNorthwest A&F UniversityNorthwest A&F UniversityNorthwest A&F UniversityNorthwest A&F UniversityPeste des petits ruminants (PPR) is an acute and highly contagious disease in small ruminants that causes significant economic losses in developing countries. An increasing number of studies have demonstrated that both autophagy and apoptosis are important cellular mechanisms for maintaining homeostasis, and they participate in the host response to pathogens. However, the crosstalk between apoptosis and autophagy in host cells during PPRV infection has not been clarified. In this study, autophagy was induced upon virus infection in caprine endometrial epithelial cells (EECs), as determined by the appearance of double- and single-membrane autophagy-like vesicles, LC3-I/LC3-II conversion, and p62 degradation. We also found that PPRV infection triggered a complete autophagic response, most likely mediated by the non-structural protein C and nucleoprotein N. Moreover, our results suggest that autophagy not only promotes the replication of PPRV in EECs but also provides a potential mechanism for inhibiting PPRV-induced apoptosis. Inhibiting autophagosome formation by wortmannin and knocking down the essential autophagic proteins Beclin-1 and ATG7 induces caspase-dependent apoptosis in EECs in PPRV infection. However, inhibiting autophagosome and lysosome fusion by NH4Cl and chloroquine did not increase the number of apoptotic cells. Collectively, these data are the first to indicate that PPRV-induced autophagy inhibits caspase-dependent apoptosis and thus contributes to the enhancement of viral replication and maturity in host cells.http://dx.doi.org/10.1080/21505594.2018.1496776Peste des petits ruminants virus (PPRV)autophagyapoptosisreplicationcaprine endometrial epithelial cells (EECs)
spellingShingle Bo Yang
Qinghong Xue
Xuefeng Qi
Xueping Wang
Peilong Jia
Shuying Chen
Ting Wang
Tianxia Xue
Jingyu Wang
Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
Virulence
Peste des petits ruminants virus (PPRV)
autophagy
apoptosis
replication
caprine endometrial epithelial cells (EECs)
title Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
title_full Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
title_fullStr Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
title_full_unstemmed Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
title_short Autophagy enhances the replication of Peste des petits ruminants virus and inhibits caspase-dependent apoptosis in vitro
title_sort autophagy enhances the replication of peste des petits ruminants virus and inhibits caspase dependent apoptosis in vitro
topic Peste des petits ruminants virus (PPRV)
autophagy
apoptosis
replication
caprine endometrial epithelial cells (EECs)
url http://dx.doi.org/10.1080/21505594.2018.1496776
work_keys_str_mv AT boyang autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT qinghongxue autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT xuefengqi autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT xuepingwang autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT peilongjia autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT shuyingchen autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT tingwang autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT tianxiaxue autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro
AT jingyuwang autophagyenhancesthereplicationofpestedespetitsruminantsvirusandinhibitscaspasedependentapoptosisinvitro