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

Xiao, Changguang; Li, Chenxi; Di, Di; Cappelle, Julien; Liu, Lihong; Wang, Xin; Pang, Linlin; Xu, Jianyun; Liu, Ke; Li, Beibei; Shao, Donghua; Qiu, Yafeng; Ren, Wei; Widén, Frederik; Chevalier, Véronique; Wei, Jianchao; Wu, Xiao-Dong; Ma, Zhiyong

doi:10.1371/journal.pntd.0007046

Cited by 30 publications

(43 citation statements)

References 31 publications

(56 reference statements)

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“…The levels of viremia in rGI-inoculated ducklings were significantly higher than those in rGIII-inoculated ducklings during the experimental period ( Fig 10C), thus suggesting that rGI replicated more efficiently than rGIII in ducklings, in agreement with previous observations [22,23]. A significant difference in viremia levels between the ducklings inoculated with the substitution mutant virus and the parental virus was observed.…”

Section: Plos Pathogenssupporting

confidence: 91%

“…These observations suggest an essential contribution of birds to the maintenance and transmission of the JEV as well as the JEV genotype shift. Indeed, GI strains have been demonstrated to replicate more efficiently than GIII strains in domestic ducklings and young chickens, thus showing an advantage of GI strains over GIII strains in replication efficiency and host adaption in birds, and contributing to the JEV genotype shift [22,23]. The mechanisms underlying this advantage are not known.…”

Section: Introductionmentioning

confidence: 99%

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NS5-V372A and NS5-H386Y variations are responsible for differences in interferon α/β induction and co-contribute to the replication advantage of Japanese encephalitis virus genotype I over genotype III in ducklings

Huang

et al. 2020

PLoS Pathog

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Japanese encephalitis virus (JEV) genotype I (GI) replicates more efficiently than genotype III (GIII) in birds, and this difference is considered to be one of the reasons for the JEV genotype shift. In this study, we utilized duck embryo fibroblasts and domestic ducklings as in vitro and in vivo models of a JEV amplifying avian host to identify the viral determinants of the differing replication efficiency between the GI and GIII strains in birds. GI strains induced significantly lower levels of interferon (IFN)-α and β production than GIII strains, an effect orrelated with the enhanced replication efficiency of GI strains over GIII strains. By using a series of chimeric viruses with exchange of viral structural and non-structural (NS) proteins, we identified NS5 as the viral determinant of the differences in IFN-α and β induction and replication efficiency between the GI and III strains. NS5 inhibited IFN-α and β production induced by poly(I:C) stimulation and harbored 11 amino acid variations, of which the NS5-V372A and NS5-H386Y variations were identified to co-contribute to the differences in IFNα and β induction and replication efficiency between the strains. The NS5-V372A and NS5-H386Y variations resulted in alterations in the number of hydrogen bonds formed with neighboring residues, which were associated with the different ability of the GI and GIII strains to inhibit IFN-α and β production. Our findings indicated that the NS5-V372A and NS5-H386Y variations enabled GI strains to inhibit IFN-α and β production more efficiently than GIII strains for antagonism of the IFN-I mediated antiviral response, thereby leading to the replication and host adaption advantages of GI strains over GIII strains in birds. These findings provide new insight into the molecular basis of the JEV genotype shift.

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Section: Plos Pathogenssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

NS5-V372A and NS5-H386Y variations are responsible for differences in interferon α/β induction and co-contribute to the replication advantage of Japanese encephalitis virus genotype I over genotype III in ducklings

Huang

et al. 2020

PLoS Pathog

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“…Regarding the influence of JEV genotype in JEV transmission risk, Xiao et al. () have shown that genotype I (the most dominant genotype in some JEV endemic regions, including China) has enhanced replication efficiency in avian hosts compared to genotype III (higher viremia titers and longer viremic duration). This has probably resulted in higher exposure and consequent infection in mosquitoes, contributing to the efficiency of the bird‐associated transmission cycle and elucidating on how JEV genotype and strain may influence the dynamics of JEV transmission (Xiao et al., ).…”

Section: Discussionmentioning

confidence: 99%

Introduction of the Japanese encephalitis virus ( JEV ) in the United States – A qualitative risk assessment

Oliveira

Piaggio

Cohnstaedt

et al. 2019

Transbound Emerg Dis

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Summary The purpose of this risk assessment (RA) was to qualitatively estimate the risk of emergence of the Japanese encephalitis virus (JEV) in the United States (US). We followed the framework for RA of emerging vector‐borne livestock diseases (de Vos et al. 2011), which consists of a structured questionnaire, whose answers to questions can be delivered in risk categories, descriptive statements, or yes or no type of answers, being supported by the literature. The most likely pathways of introduction of JEV identified were: (a) entry through infected vectors (by aircraft, cargo ships, tires, or wind); (b) import of infected viremic animals; (c) entry of viremic migratory birds; (d) import of infected biological materials; (e) import of infected animal products; (f) entry of infected humans; and (g) import/production of contaminated biological material (e.g., vaccines). From these pathways, the probability of introduction of JEV through infected adult mosquitoes via aircraft was considered very high and via ships/containers was deemed low to moderate. The probability of introduction via other pathways or modes of entry (vector eggs or larvae, hosts, and vaccines) was considered negligible. The probability of transmission of JEV was variable, ranging from low to high (in the presence of both competent vectors and hosts), depending on the area of introduction within the US. Lastly, the probability of establishment of JEV in the continental US was considered negligible. For that reason, we stopped the risk assessment at this point of the framework. This RA provides important information regarding the elements that contribute to the risk associated with the introduction of JEV in the US. This RA also indicates that infected mosquitoes transported in aircraft (and cargo ships) are the most likely pathway of JEV entry and therefore, mitigation strategies should be directed towards this pathway.

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“…Other studies compared replication efficiency of GI isolates to GIII isolates. Depending on the study, GI was shown to replicate more efficiently in pig, avian, and mosquito cells than GIII (10,47,48). Genotype I had a higher infection rate and shorter extrinsic incubation period than GIII during in vivo studies using C. quinquefasciatus (12).…”

Section: Jev Genomics and Phylogenymentioning

confidence: 98%

“…Having expanded from Japan, where it was first isolated, JEV has spread to all neighboring countries, now covering most regions in Southeast Asia. Besides the wide distribution of JEV, recent evidence of geographical genotype displacement has pointed to the changing dynamics of JEV transmission, raising public health concern regarding virus spread to susceptible regions of the globe (4,(10)(11)(12). Japanese encephalitis virus genetic material has already been identified in mosquitoes and birds collected in northern Italy, where human cases are unreported to date (13,14); concurrently, other arboviruses have been emerging in previously unaffected areas, with one of the most recent examples being the occurrence of outbreaks of Zika (although humans are reservoir of this virus) virus in South America (15).…”

Section: Introductionmentioning

confidence: 99%

Perspectives Regarding the Risk of Introduction of the Japanese Encephalitis Virus (JEV) in the United States

et al. 2020

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Japanese encephalitis (JE) is a zoonotic, emerging disease transmitted by mosquito vectors infected with the Japanese encephalitis virus (JEV). Its potential for emergence into susceptible regions is high, including in the United States (US), and is a reason of economic concern among the agricultural community, and to public health due to high morbidity and mortality rates in humans. While exploring the complexities of interactions involved with viral transmission, we proposed a new outlook on the role of vectors, hosts and the environment under changing conditions. For instance, the role of feral pigs may have been underappreciated in our previous work, given research keeps pointing to the importance of susceptible populations of wild swine in naïve regions as key elements for the introduction of emergent vector-borne diseases. High risk of JEV introduction has been associated with the transportation of infected mosquitoes via aircraft. Nonetheless, no JEV outbreaks have been reported in the US to date and results from a qualitative risk assessment considered the risk of establishment to be negligible under the current conditions (environmental, vector, pathogen, and host). In this work, we discuss virus-vector-host interactions and ecological factors important for virus transmission and spread, review research on the risk of JEV introduction to the US considering the implications of risk dismissal as it relates to past experiences with similar arboviruses, and reflect on future directions, challenges, and implications of a JEV incursion.

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

Cited by 30 publications

References 31 publications

NS5-V372A and NS5-H386Y variations are responsible for differences in interferon α/β induction and co-contribute to the replication advantage of Japanese encephalitis virus genotype I over genotype III in ducklings

NS5-V372A and NS5-H386Y variations are responsible for differences in interferon α/β induction and co-contribute to the replication advantage of Japanese encephalitis virus genotype I over genotype III in ducklings

Introduction of the Japanese encephalitis virus ( JEV ) in the United States – A qualitative risk assessment

Perspectives Regarding the Risk of Introduction of the Japanese Encephalitis Virus (JEV) in the United States

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