A single mutation in the cis-acting replication element identified within the EV-A71 2C-coding region causes defects in virus production in cell culture

References

• Solomon T, Lewthwaite P, Perera D, et al. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10(11):778–790. doi:https://doi.org/10.1016/S1473-3099(10)70194-8.
   PubMed Web of Science ®Google Scholar
• Xing W, Liao Q, Viboud C, et al. Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis. 2014;14(4):308–318. doi:https://doi.org/10.1016/S1473-3099(13)70342-6.
   PubMed Web of Science ®Google Scholar
• Xu J, Qian Y, Wang S, et al. EV71: an emerging infectious disease vaccine target in the Far east. Vaccine. 2010 Apr 30;28(20):3516–3521. doi:https://doi.org/10.1016/j.vaccine.2010.03.003.
   PubMed Web of Science ®Google Scholar
• Chang LY, Huang L-M, Gau SS-F, et al. Neurodevelopment and cognition in children after enterovirus 71 infection. N Engl J Med. 2007;356(12):1226–1234. doi:https://doi.org/10.1056/NEJMoa065954.
   PubMed Web of Science ®Google Scholar
• Liang L, Cheng Y, Li Y, et al. Long-term neurodevelopment outcomes of hand, foot and mouth disease inpatients infected with EV-A71 or CV-A16, a retrospective cohort study. Emerg Microbes Infect. 2021;10(1):545–554. doi:https://doi.org/10.1080/22221751.2021.1901612.
   PubMed Web of Science ®Google Scholar
• Huang CC, Liu CC, Chang YC, et al. Neurologic complications in children with enterovirus 71 infection. Engl J Med. 1999;341(13):936–942. doi:https://doi.org/10.1056/NEJM199909233411302.
   PubMed Web of Science ®Google Scholar
• Koyuncu OO, Hogue IB, Enquist LW. Virus infections in the nervous system. Cell Host Microbe. 2013;13(4):379–393. doi:https://doi.org/10.1016/j.chom.2013.03.010.
   PubMed Web of Science ®Google Scholar
• Teoh HL, Mohammad SS, Britton PN, et al. Clinical characteristics and functional motor outcomes of enterovirus 71 neurological disease in children. JAMA Neurol. 2016;73(3):300–307. doi:https://doi.org/10.1001/jamaneurol.2015.4388.
   PubMed Web of Science ®Google Scholar
• McMinn PC. Recent advances in the molecular epidemiology and control of human enterovirus 71 infection. Curr Opin Virol. 2012;2(2):199–205. doi:https://doi.org/10.1016/j.coviro.2012.02.009.
   PubMed Web of Science ®Google Scholar
• Puenpa J, Wanlapakorn N, Vongpunsawad S, et al. The history of enterovirus A71 outbreaks and molecular epidemiology in the Asia-Pacific region. J Biomed Sci. 2019;26(1):75, doi:https://doi.org/10.1186/s12929-019-0573-2.
   PubMed Web of Science ®Google Scholar
• Bessaud M, Pillet S, Ibrahim W, et al. Molecular characterization of human enteroviruses in the Central African Republic: uncovering wide diversity and identification of a new human enterovirus A71 genogroup. J Clin Microbiol. 2012;50(5):1650–1658. doi:https://doi.org/10.1128/JCM.06657-11.
   Web of Science ®Google Scholar
• Bessaud M, Razafindratsimandresy R, Nougairède A, et al. Molecular comparison and evolutionary analyses of VP1 nucleotide sequences of new African human enterovirus 71 isolates reveal a wide genetic diversity. PLoS One. 2014;9(3):e90624, doi:https://doi.org/10.1371/journal.pone.0090624.
   PubMed Web of Science ®Google Scholar
• Saxena VK, Sane S, Nadkarni SS, et al. Genetic diversity of enterovirus A71, India. Emerg Infect Dis. 2015;21(1):123–126. doi:https://doi.org/10.3201/eid2101.140743.
   Web of Science ®Google Scholar
• van der Sanden S, Koopmans M, Uslu G, et al. Epidemiology of enterovirus 71 in The Netherlands, 1963 to 2008. J Clin Microbiol. 2009;47(9):2826–2833. doi:https://doi.org/10.1128/JCM.00507-09.
   PubMed Web of Science ®Google Scholar
• Lin JY, Chen TC, Weng KF, et al. Viral and host proteins involved in picornavirus life cycle. J Biomed Sci. 2009;16(1):103, doi:https://doi.org/10.1186/1423-0127-16-103.
   Google Scholar
• Wang H, Li Y. Recent progress on functional genomics research of enterovirus 71. Virol Sin. 2019;34(1):9–21. doi:https://doi.org/10.1007/s12250-018-0071-9.
   PubMed Web of Science ®Google Scholar
• Kao CC, Singh P, Ecker DJ. De Novo initiation of viral RNA-dependent RNA synthesis. Virology. 2001;287(2):251–260. doi:https://doi.org/10.1006/viro.2001.1039.
   PubMed Web of Science ®Google Scholar
• Beerens N, Selisko B, Ricagno S, et al. De Novo initiation of RNA synthesis by the arterivirus RNA-dependent RNA polymerase. J Virol. 2007;81:8384–8395. doi:https://doi.org/10.1128/JVI.00564-07.
   Web of Science ®Google Scholar
• Nagy PD, Carpenter CD, Simon AE. A novel 3’ -end repair mechanism in an RNA virus. Proc Natl Acad Sci USA. 1997;94(4):1113–1118. doi:https://doi.org/10.1073/pnas.94.4.1113.
   Web of Science ®Google Scholar
• Paul AV, van Boom JH, Filippov D, et al. Protein-primed RNA synthesis by purified poliovirus RNA polymerase. Nature. 1998;393(6682):280–284. doi:https://doi.org/10.1038/30529.
   PubMed Web of Science ®Google Scholar
• Yang Y, Rijnbrand R, McKnight KL, et al. Sequence requirements for viral RNA replication and VPg uridylylation directed by the internal cis-acting replication element (cre) of human rhinovirus type 14. J Virol. 2002;76(15):7485–7494. doi:https://doi.org/10.1128/jvi.76.15.7485-7494.2002.
   Web of Science ®Google Scholar
• Paul AV, Yin J, Mugavero J, et al. A “slide-back” mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus. J Biol Chem. 2003;278(45):43951–43960. doi:https://doi.org/10.1074/jbc.M307441200.
   PubMed Web of Science ®Google Scholar
• Yin J, Paul AV, Wimmer E, et al. Functional dissection of a poliovirus cis-acting replication element [PV-cre(2C)]: analysis of single- and dual-cre viral genomes and proteins that bind specifically to PV-cre RNA. J Virol. 2003;77(9):5152–5166. doi:https://doi.org/10.1128/jvi.77.9.5152-5166.2003.
   Web of Science ®Google Scholar
• Mason PW, Bezborodova SV, Henry TM. Identification and characterization of a cis-acting replication element (cre) adjacent to the internal ribosome entry site of foot-and-mouth disease virus. J Virol. 2002;76(19):9686–9694. doi:https://doi.org/10.1128/jvi.76.19.9686-9694.2002.
   Web of Science ®Google Scholar
• McKnight KL, Lemon SM. The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication. RNA. 1998;4(12):1569–1584. doi:https://doi.org/10.1017/s1355838298981006.
   Web of Science ®Google Scholar
• Lobert PE, Escriou N, Ruelle J, et al. A coding RNA sequence acts as a replication signal in cardioviruses. Proc Natl Acad Sci USA. 1999;96(20):11560–11565. doi:https://doi.org/10.1073/pnas.96.20.11560.
   Web of Science ®Google Scholar
• Goodfellow I, Chaudhry Y, Richardson A, et al. Identification of a cis-acting replication element within the poliovirus coding region. J Virol. 2000;74(10):4590–4600. doi:https://doi.org/10.1128/jvi.74.10.4590-4600.2000.
   Web of Science ®Google Scholar
• Rieder E, Paul AV, Kim DW, et al. Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation. J Virol. 2000;74(22):10371–10380. doi:https://doi.org/10.1128/jvi.74.22.10371-10380.2000.
   Web of Science ®Google Scholar
• van Ooij MJ M, Vogt DA, Paul A, et al. Structural and functional characterization of the coxsackievirus B3 CRE(2C): role of CRE(2C) in negative- and positive-strand RNA synthesis. J Gen Virol. 2006;87(Pt 1):103–113. doi:https://doi.org/10.1099/vir.0.81297-0.
   Google Scholar
• Gerber K, Wimmer E, Paul AV. Biochemical and genetic studies of the initiation of human rhinovirus 2 RNA replication: identification of a cis-replicating element in the coding sequence of 2A(pro). J Virol. 2001;75(22):10979–10990. doi:https://doi.org/10.1128/JVI.75.22.10979-10990.2001.
   Web of Science ®Google Scholar
• Yang Y, Yi M, Evans DJ, et al. Identification of a conserved RNA replication element (cre) within the 3Dpol-coding sequence of hepatoviruses. J Virol. 2008;82(20):10118–10128. doi:https://doi.org/10.1128/JVI.00787-08.
   Web of Science ®Google Scholar
• Zhao J, Qiu J, Aryal S, et al. The RNA architecture of the SARS-CoV-2 3'-untranslated region. Viruses. 2020;12(12):1473, doi:https://doi.org/10.3390/v12121473.
   Web of Science ®Google Scholar
• Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics. 2010;11:129, doi:https://doi.org/10.1186/1471-2105-11-129.
   PubMed Web of Science ®Google Scholar
• Steil BP, Barton DJ. Cis-active RNA elements (CREs) and picornavirus RNA replication. Virus Res. 2009;139(2):240–252. doi:https://doi.org/10.1016/j.virusres.2008.07.027.
   PubMed Web of Science ®Google Scholar
• Arita M, Shimizu H, Nagata N, et al. Temperature-sensitive mutants of enterovirus 71 show attenuation in cynomolgus monkeys. J Gen Virol. 2005;86(Pt 5):1391–1401. doi:https://doi.org/10.1099/vir.0.80784-0.
   PubMed Web of Science ®Google Scholar
• Phuektes P, Chua BH, Sanders S, et al. Mapping genetic determinants of the cell-culture growth phenotype of enterovirus 71. J Gen Virol. 2011;92(Pt 6):1380–1390. doi:https://doi.org/10.1099/vir.0.029371-0.
   PubMedGoogle Scholar
• Shang B, Deng C, Ye H, et al. Development and characterization of a stable eGFP enterovirus 71 for antiviral screening. Antiviral Res. 2013;97(2):198–205. doi:https://doi.org/10.1016/j.antiviral.2012.12.010.
   PubMed Web of Science ®Google Scholar
• Zhang H, Song Z, Zou J, et al. An infectious clone of enterovirus 71(EV71) that is capable of infecting neonatal immune competent mice without adaptive mutations. Emerg Microbes Infect. 2020;9(1):427–438. doi:https://doi.org/10.1080/22221751.2020.1729665.
   PubMed Web of Science ®Google Scholar
• Ke X, Zhang Y, Liu Y, et al. A single mutation in the VP1 gene of enterovirus 71 enhances viral binding to heparan sulfate and impairs viral pathogenicity in mice. Viruses. 2020;12(8):883, doi:https://doi.org/10.3390/v12080883.
   Web of Science ®Google Scholar
• Pfister T, Wimmer E. Characterization of the nucleotide triphosphatase activity of poliovirus protein 2C reveals a mechanism by which guanidine inhibits replication of poliovirus. J Biol Chem. 1999;274(11):6992–7001. doi:https://doi.org/10.1074/jbc.274.11.6992.
   Web of Science ®Google Scholar
• Shih S, Stollar V, Li M. Host factors in enterovirus 71 replication. J Virol. 2011;85(19):9658–9666. doi:https://doi.org/10.1128/JVI.05063-11.
   PubMed Web of Science ®Google Scholar
• Brunner J, Nguyen J, Roehl H, et al. Functional interaction of heterogeneous nuclear ribonucleoprotein C with poliovirus RNA synthesis initiation complexes. J Virol. 2005;79(6):3254–3266. doi:https://doi.org/10.1128/JVI.79.6.3254-3266.2005.
   PubMed Web of Science ®Google Scholar
• Wu K, Phuektes P, Pankaj Kumar P, et al. Human genome-wide RNAi screen reveals host factors required for enterovirus 71 replication. J Virol Nat Commun. 2016;7:13150, doi:https://doi.org/10.1038/ncomms13150.
   PubMed Web of Science ®Google Scholar
• Huang P, Jheng J, Arnold J, et al. UGGT1 enhances enterovirus 71 pathogenicity by promoting viral RNA synthesis and viral replication. PLoS Pathog. 2017;13(5):e1006375, doi:https://doi.org/10.1371/journal.ppat.1006375.
   Web of Science ®Google Scholar
• Liu F, Zhou S, Deng Y, et al. MiR-216b is involved in pathogenesis and progression of hepatocellular carcinoma through HBx-miR-216b- IGF2BP2 signaling pathway. Cell Death Dis. 2015;6(3):e1670, doi:https://doi.org/10.1038/cddis.2015.46.
   PubMedGoogle Scholar
• Chatel-Chaix L, Germain M, Motorina A, et al. A host YB-1 ribonucleoprotein complex is hijacked by hepatitis C virus for the control of NS3-dependent particle production. J Virol. 2013;87(21):11704–11720. doi:https://doi.org/10.1128/JVI.01474-13.
   Web of Science ®Google Scholar
• Watanabe T, Kawakami E, Shoemaker JE, et al. Influenza virus-host interactome screen as a platform for antiviral drug development. Cell Host Microbe. 2014;16(6):795–805. doi:https://doi.org/10.1016/j.chom.2014.11.002.
   PubMed Web of Science ®Google Scholar
• Ertel KJ, Brunner JE, Semler BL. Mechanistic consequences of hnRNP C binding to both RNA termini of poliovirus negative-strand RNA intermediates. J Virol. 2010;84(9):4229–4242. doi:https://doi.org/10.1128/JVI.02198-09.
   PubMed Web of Science ®Google Scholar