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Genome Replication and Regulation of Viral Gene Expression

cis-Acting Sequences and Secondary Structures in Untranslated Regions of Duck Tembusu Virus RNA Are Important for Cap-Independent Translation and Viral Proliferation

Tao Wang, Andres Merits, Yuanyuan Wu, Mingshu Wang, Renyong Jia, Dekang Zhu, Mafeng Liu, Xinxin Zhao, Qiao Yang, Ying Wu, Shaqiu Zhang, Yunya Liu, Ling Zhang, Yanling Yu, Leichang Pan, Shun Chen, Anchun Cheng
Julie K. Pfeiffer, Editor
Tao Wang
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Andres Merits
dInstitute of Technology, University of Tartu, Tartu, Estonia
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Yuanyuan Wu
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Mingshu Wang
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Renyong Jia
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Dekang Zhu
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Mafeng Liu
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Xinxin Zhao
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Qiao Yang
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Ying Wu
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Shaqiu Zhang
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Yunya Liu
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Ling Zhang
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Yanling Yu
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Leichang Pan
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
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Shun Chen
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Anchun Cheng
aInstitute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
bResearch Center of Avian Disease, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China
cKey Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu, Sichuan, China
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Julie K. Pfeiffer
University of Texas Southwestern Medical Center
Roles: Editor
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DOI: 10.1128/JVI.00906-20
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ABSTRACT

Duck Tembusu virus (DTMUV) (genus Flavivirus) is a causative agent of duck egg drop syndrome and has zoonotic potential. The positive-strand RNA genomes of flaviviruses are commonly translated in a cap-dependent manner. However, dengue and Zika viruses also exhibit cap-independent translation. In this study, we show that RNAs containing 5′ and 3′ untranslated regions (UTRs) of DTMUV, mosquito-borne Tembusu virus (TMUV), and Japanese encephalitis virus can be translated in a cap-independent manner in mammalian, avian, and mosquito cells. The ability of the 5′ UTRs of flaviviruses to direct the translation of a second open reading frame in bicistronic RNAs was much less than that observed for internal ribosome entry site (IRES) encephalomyocarditis virus, indicating a lack of substantial IRES activity. Instead, cap-independent translation of DTMUV RNA was dependent on the presence of a 3′ UTR, RNA secondary structures located in both UTRs, and specific RNA sequences. Mutations inhibiting cap-independent translation decreased DTMUV proliferation in vitro and delayed, but did not prevent, the death of infected duck embryos. Thus, the 5′ and 3′ UTRs of DTMUV enable the virus to use a cap- and IRES-independent RNA genome translation strategy that is important for its propagation and virulence.

IMPORTANCE The genus Flavivirus includes major human pathogens, as well as animal-infecting viruses with zoonotic potential. In order to counteract the threats these viruses represent, it is important to understand their basic biology to develop universal attenuation strategies. Here, we demonstrate that five different flaviviruses use cap-independent translation, indicating that the phenomenon is probably common to all members of the genus. The mechanism used for flavivirus cap-independent translation was found to be different from that of IRES-mediated translation and dependent on both 5′ and 3′ UTRs that act in cis. As cap-independent translation was also observed in mosquito cells, its role in flavivirus infection is unlikely to be limited to the evasion of consequences of the shutoff of host translation. We found that the inhibition of cap-independent translation results in decreased viral proliferation, indicating that the strategy could be applied to produce attenuated variants of flaviviruses as potential vaccine candidates.

  • Copyright © 2020 American Society for Microbiology.

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cis-Acting Sequences and Secondary Structures in Untranslated Regions of Duck Tembusu Virus RNA Are Important for Cap-Independent Translation and Viral Proliferation
Tao Wang, Andres Merits, Yuanyuan Wu, Mingshu Wang, Renyong Jia, Dekang Zhu, Mafeng Liu, Xinxin Zhao, Qiao Yang, Ying Wu, Shaqiu Zhang, Yunya Liu, Ling Zhang, Yanling Yu, Leichang Pan, Shun Chen, Anchun Cheng
Journal of Virology Jul 2020, 94 (16) e00906-20; DOI: 10.1128/JVI.00906-20

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cis-Acting Sequences and Secondary Structures in Untranslated Regions of Duck Tembusu Virus RNA Are Important for Cap-Independent Translation and Viral Proliferation
Tao Wang, Andres Merits, Yuanyuan Wu, Mingshu Wang, Renyong Jia, Dekang Zhu, Mafeng Liu, Xinxin Zhao, Qiao Yang, Ying Wu, Shaqiu Zhang, Yunya Liu, Ling Zhang, Yanling Yu, Leichang Pan, Shun Chen, Anchun Cheng
Journal of Virology Jul 2020, 94 (16) e00906-20; DOI: 10.1128/JVI.00906-20
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KEYWORDS

duck Tembusu virus
cap-independent translation
secondary structure
Untranslated Regions

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