Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.

Japanese encephalitis virus (JEV) genotype dominance has shifted to genotype I (GI) from genotype III (GIII) in China as demonstrated by molecular epidemiological surveillance. In this study, we performed a serological survey in JEV-non-vaccinated pigs to confirm JEV genotype shift at the sero-epide...

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Published in:PLOS Neglected Tropical Diseases
Main Authors: Changguang Xiao, Chenxi Li, Di Di, Julien Cappelle, Lihong Liu, Xin Wang, Linlin Pang, Jinpeng Xu, Ke Liu, Beibei Li, Donghua Shao, Yafeng Qiu, Weijie Ren, Frederik Widén, Véronique Chevalier, Jianchao Wei, Xiaodong Wu, Zhiyong Ma
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2018
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0007046
https://doaj.org/article/a403a069b033440d9ad9dfa5c05d5bb1
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spelling ftdoajarticles:oai:doaj.org/article:a403a069b033440d9ad9dfa5c05d5bb1 2023-05-15T15:15:32+02:00 Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings. Changguang Xiao Chenxi Li Di Di Julien Cappelle Lihong Liu Xin Wang Linlin Pang Jinpeng Xu Ke Liu Beibei Li Donghua Shao Yafeng Qiu Weijie Ren Frederik Widén Véronique Chevalier Jianchao Wei Xiaodong Wu Zhiyong Ma 2018-12-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0007046 https://doaj.org/article/a403a069b033440d9ad9dfa5c05d5bb1 EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0007046 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0007046 https://doaj.org/article/a403a069b033440d9ad9dfa5c05d5bb1 PLoS Neglected Tropical Diseases, Vol 12, Iss 12, p e0007046 (2018) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2018 ftdoajarticles https://doi.org/10.1371/journal.pntd.0007046 2022-12-31T07:51:10Z Japanese encephalitis virus (JEV) genotype dominance has shifted to genotype I (GI) from genotype III (GIII) in China as demonstrated by molecular epidemiological surveillance. In this study, we performed a serological survey in JEV-non-vaccinated pigs to confirm JEV genotype shift at the sero-epidemiological level. The average ratio of GI/GIII infection was 1.87, suggesting co-circulation of GI and GIII infections with GI infection being more prevalent in pigs in China. To gain an insight into the reasons for this JEV genotype shift, the replication kinetics of seven recently-isolated JEV isolates including three GI strains and four GIII strains were compared in mosquito C6/36 cells, chicken fibroblast cells (DF-1) and porcine iliac artery endothelial cells (PIEC). We observed that GI strains replicated more efficiently than GIII strains in DF-1 and PIEC cells, particularly in DF-1 cells with titers reaching 22.9-225.3 fold higher than GIII strains. This shows an enhanced replication efficiency of GI viruses in avian cells. To examine this enhanced replication efficiency in vivo, young domestic ducklings were used as the animal model and inoculated with GI and GIII strains at day 2 post-hatching. We observed that GI-inoculated ducklings developed higher viremia titers and displayed a comparatively longer viremic duration than GIII-inoculated ducklings. These results conform to the hypothesis of an enhanced replication efficiency for GI viruses in birds. There are 36 amino acid differences between GI and GIII viruses, some of which may be responsible for the enhanced replication efficiency of GI viruses in birds. Based on these findings, we speculated that the enhanced replication of GI viruses in birds would have resulted in higher exposure and therefore infection in mosquitoes, which could result in an increased transmission efficiency of GI viruses in the birds-mosquitoes-birds enzootic transmission cycle, thereby contributing to JEV genotype shift. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 12 12 e0007046
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Changguang Xiao
Chenxi Li
Di Di
Julien Cappelle
Lihong Liu
Xin Wang
Linlin Pang
Jinpeng Xu
Ke Liu
Beibei Li
Donghua Shao
Yafeng Qiu
Weijie Ren
Frederik Widén
Véronique Chevalier
Jianchao Wei
Xiaodong Wu
Zhiyong Ma
Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description Japanese encephalitis virus (JEV) genotype dominance has shifted to genotype I (GI) from genotype III (GIII) in China as demonstrated by molecular epidemiological surveillance. In this study, we performed a serological survey in JEV-non-vaccinated pigs to confirm JEV genotype shift at the sero-epidemiological level. The average ratio of GI/GIII infection was 1.87, suggesting co-circulation of GI and GIII infections with GI infection being more prevalent in pigs in China. To gain an insight into the reasons for this JEV genotype shift, the replication kinetics of seven recently-isolated JEV isolates including three GI strains and four GIII strains were compared in mosquito C6/36 cells, chicken fibroblast cells (DF-1) and porcine iliac artery endothelial cells (PIEC). We observed that GI strains replicated more efficiently than GIII strains in DF-1 and PIEC cells, particularly in DF-1 cells with titers reaching 22.9-225.3 fold higher than GIII strains. This shows an enhanced replication efficiency of GI viruses in avian cells. To examine this enhanced replication efficiency in vivo, young domestic ducklings were used as the animal model and inoculated with GI and GIII strains at day 2 post-hatching. We observed that GI-inoculated ducklings developed higher viremia titers and displayed a comparatively longer viremic duration than GIII-inoculated ducklings. These results conform to the hypothesis of an enhanced replication efficiency for GI viruses in birds. There are 36 amino acid differences between GI and GIII viruses, some of which may be responsible for the enhanced replication efficiency of GI viruses in birds. Based on these findings, we speculated that the enhanced replication of GI viruses in birds would have resulted in higher exposure and therefore infection in mosquitoes, which could result in an increased transmission efficiency of GI viruses in the birds-mosquitoes-birds enzootic transmission cycle, thereby contributing to JEV genotype shift.
format Article in Journal/Newspaper
author Changguang Xiao
Chenxi Li
Di Di
Julien Cappelle
Lihong Liu
Xin Wang
Linlin Pang
Jinpeng Xu
Ke Liu
Beibei Li
Donghua Shao
Yafeng Qiu
Weijie Ren
Frederik Widén
Véronique Chevalier
Jianchao Wei
Xiaodong Wu
Zhiyong Ma
author_facet Changguang Xiao
Chenxi Li
Di Di
Julien Cappelle
Lihong Liu
Xin Wang
Linlin Pang
Jinpeng Xu
Ke Liu
Beibei Li
Donghua Shao
Yafeng Qiu
Weijie Ren
Frederik Widén
Véronique Chevalier
Jianchao Wei
Xiaodong Wu
Zhiyong Ma
author_sort Changguang Xiao
title Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
title_short Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
title_full Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
title_fullStr Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
title_full_unstemmed Differential replication efficiencies between Japanese encephalitis virus genotype I and III in avian cultured cells and young domestic ducklings.
title_sort differential replication efficiencies between japanese encephalitis virus genotype i and iii in avian cultured cells and young domestic ducklings.
publisher Public Library of Science (PLoS)
publishDate 2018
url https://doi.org/10.1371/journal.pntd.0007046
https://doaj.org/article/a403a069b033440d9ad9dfa5c05d5bb1
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 12, Iss 12, p e0007046 (2018)
op_relation https://doi.org/10.1371/journal.pntd.0007046
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0007046
https://doaj.org/article/a403a069b033440d9ad9dfa5c05d5bb1
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