Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus
Abstract
During the replication cycle of double-stranded (ds) RNA viruses, the viral RNA-dependent RNA polymerase (RdRP) replicates and transcribes the viral genome from within the viral capsid. How the RdRP molecules are packaged within the virion and how they function within the confines of an intact capsid are intriguing questions with answers that most likely vary across the different dsRNA virus families. In this study, we have determined a 2.4 Å resolution structure of an RdRP from the human picobirnavirus (hPBV). In addition to the conserved polymerase fold, the hPBV RdRP possesses a highly flexible 24 amino acid loop structure located near the C-terminus of the protein that is inserted into its active site. In vitro RNA polymerization assays and site-directed mutagenesis showed that: (1) the hPBV RdRP is fully active using both ssRNA and dsRNA templates; (2) the insertion loop likely functions as an assembly platform for the priming nucleotide to allow de novo initiation; (3) RNA transcription by the hPBV RdRP proceeds in a semi-conservative manner; and (4) the preference of virus-specific RNA during transcription is dictated by the lower melting temperature associated with the terminal sequences. Co-expression of the hPBV RdRP and the capsid protein (CP) indicated that,more »
- Authors:
-
- Rice Univ., Houston, TX (United States)
- Univ. of Helsinki (Finland)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- Gulf Coast Consortia; Viikki Doctoral Programme in Molecular Biosciences; National Institutes of Health (NIH); Welch Foundation; Academy of Finland; Sigrid Jusélius Foundation
- OSTI Identifier:
- 1438860
- Grant/Contract Number:
- AIO67638 to YJT; C-1565; 250113; 256069; 283192
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 4; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Polymerases; Viral packaging; RNA synthesis; dsRNA viruses; Viral structure; Sequence motif analysis; RNA structure; Viral genomics
Citation Formats
Collier, Aaron M., Lyytinen, Outi L., Guo, Yusong R., Toh, Yukimatsu, Poranen, Minna M., and Tao, Yizhi J. Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus. United States: N. p., 2016.
Web. doi:10.1371/journal.ppat.1005523.
Collier, Aaron M., Lyytinen, Outi L., Guo, Yusong R., Toh, Yukimatsu, Poranen, Minna M., & Tao, Yizhi J. Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus. United States. https://doi.org/10.1371/journal.ppat.1005523
Collier, Aaron M., Lyytinen, Outi L., Guo, Yusong R., Toh, Yukimatsu, Poranen, Minna M., and Tao, Yizhi J. Thu .
"Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus". United States. https://doi.org/10.1371/journal.ppat.1005523. https://www.osti.gov/servlets/purl/1438860.
@article{osti_1438860,
title = {Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus},
author = {Collier, Aaron M. and Lyytinen, Outi L. and Guo, Yusong R. and Toh, Yukimatsu and Poranen, Minna M. and Tao, Yizhi J.},
abstractNote = {During the replication cycle of double-stranded (ds) RNA viruses, the viral RNA-dependent RNA polymerase (RdRP) replicates and transcribes the viral genome from within the viral capsid. How the RdRP molecules are packaged within the virion and how they function within the confines of an intact capsid are intriguing questions with answers that most likely vary across the different dsRNA virus families. In this study, we have determined a 2.4 Å resolution structure of an RdRP from the human picobirnavirus (hPBV). In addition to the conserved polymerase fold, the hPBV RdRP possesses a highly flexible 24 amino acid loop structure located near the C-terminus of the protein that is inserted into its active site. In vitro RNA polymerization assays and site-directed mutagenesis showed that: (1) the hPBV RdRP is fully active using both ssRNA and dsRNA templates; (2) the insertion loop likely functions as an assembly platform for the priming nucleotide to allow de novo initiation; (3) RNA transcription by the hPBV RdRP proceeds in a semi-conservative manner; and (4) the preference of virus-specific RNA during transcription is dictated by the lower melting temperature associated with the terminal sequences. Co-expression of the hPBV RdRP and the capsid protein (CP) indicated that, under the conditions used, the RdRP could not be incorporated into the recombinant capsids in the absence of the viral genome. Additionally, the hPBV RdRP exhibited higher affinity towards the conserved 5’-terminal sequence of the viral RNA, suggesting that the RdRP molecules may be encapsidated through their specific binding to the viral RNAs during assembly.},
doi = {10.1371/journal.ppat.1005523},
journal = {PLoS Pathogens},
number = 4,
volume = 12,
place = {United States},
year = {Thu Apr 14 00:00:00 EDT 2016},
month = {Thu Apr 14 00:00:00 EDT 2016}
}
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- Sun, Xiaoyu; Ilca, Serban L.; Huiskonen, Juha T.
- mBio, Vol. 9, Issue 5