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Molecular Insights Into Evolution, Mutations and Receptor‑Binding Specificity of Influenza a and B Viruses from Outpatients and Hospitalized Patients in Singapore

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Molecular Insights Into Evolution, Mutations and Receptor‑Binding Specificity of Influenza a and B Viruses from Outpatients and Hospitalized Patients in Singapore This document is downloaded from DR‑NTU (https://dr.ntu.edu.sg) Nanyang Technological University, Singapore. Molecular insights into evolution, mutations and receptor‑binding specificity of influenza A and B viruses from outpatients and hospitalized patients in Singapore Ivan, Fransiskus Xaverius; Zhou, Xinrui; Lau, Suk Hiang; Rashid, Shamima; Teo, Jasmine S. M.; Lee, Hong Kai; Koay, Evelyn S.; Chan, Kwai Peng; Leo, Yee Sin; Chen, Mark I. Cheng; Kwoh, Chee Keong; Chow, Vincent T. 2019 Ivan, F. X., Zhou, X., Lau, S. H., Rashid, S., Teo, J. S. M., Lee, H. K., . Chow, V. T. (2020). Molecular insights into evolution, mutations and receptor‑binding specificity of influenza A and B viruses from outpatients and hospitalized patients in Singapore. International Journal of Infectious Diseases, 90, 84‑96. doi:10.1016/j.ijid.2019.10.024 https://hdl.handle.net/10356/142170 https://doi.org/10.1016/j.ijid.2019.10.024 © 2019 The Authors (Published by Elsevier Ltd on behalf of International Society for Infectious Diseases). This is an open access article under the CC BY‑NC‑ND license (http://creativecommons.org/licenses/by‑nc‑nd/4.0/). Downloaded on 25 Sep 2021 02:27:31 SGT International Journal of Infectious Diseases 90 (2020) 84–96 Contents lists available at ScienceDirect International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid Molecular insights into evolution, mutations and receptor-binding specificity of influenza A and B viruses from outpatients and hospitalized patients in Singapore a,1 a,1 b,1 a Fransiskus X. Ivan , Xinrui Zhou , Suk Hiang Lau , Shamima Rashid , b c,d c,e f g Jasmine S.M. Teo , Hong Kai Lee , Evelyn S. Koay , Kwai Peng Chan , Yee Sin Leo , g,h a, b, Mark I.C. Chen , Chee Keong Kwoh *, Vincent T. Chow * a School of Computer Science and Engineering, Nanyang Technological University, Singapore b Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore c Molecular Diagnosis Centre, National University Hospital, Singapore d Singapore Immunology Network, Agency for Science, Technology and Research, Singapore e Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore f Department of Pathology, Singapore General Hospital, Singapore g National Centre for Infectious Diseases, Singapore h Saw Swee Hock School of Public Health, National University of Singapore, Singapore A R T I C L E I N F O A B S T R A C T Article history: Background: This study compared the genomes of influenza viruses that caused mild infections among Received 4 July 2019 outpatients and severe infections among hospitalized patients in Singapore, and characterized their Received in revised form 16 October 2019 molecular evolution and receptor-binding specificity. Accepted 18 October 2019 Methods: The complete genomes of influenza A/H1N1, A/H3N2 and B viruses that caused mild infections Corresponding Editor: Eskild Petersen, Aar- among outpatients and severe infections among inpatients in Singapore during 2012–2015 were hus, Denmark sequenced and characterized. Using various bioinformatics approaches, we elucidated their evolutionary, mutational and structural patterns against the background of global and vaccine strains. Keywords: Results: The phylogenetic trees of the 8 gene segments revealed that the outpatient and inpatient strains Influenza overlapped with representative global and vaccine strains. We observed a cluster of inpatients with A/H3N2 A/H1N1 viruses A/H3N2 viruses strains that were closely related to vaccine strain A/Texas/50/2012(H3N2). Several protein sites could Influenza B accurately discriminate between outpatient versus inpatient strains, with site 221 in neuraminidase (NA) Evolution achieving the highestaccuracyfor A/H3N2.Interestingly, amino acid residues ofinpatient but notoutpatient Mutations isolates at those sites generally matched the corresponding residues in vaccine strains, except at site 145 of Receptor binding hemagglutinin (HA).Thiswould beespecially relevantforfuturesurveillanceof A/H3N2strains inrelationto Severity their antigenicity and virulence. Furthermore, we observed a trend in which the HA proteins of influenza A/ Singapore H3N2 and A/H1N1 exhibited enhanced ability to bind both avian and human host cell receptors. In contrast, the binding ability to each receptor was relatively stable for the HA of influenza B. Conclusions: Overall, our findings extend our understanding of the molecular and structural evolution of influenza virus strains in Singapore within the global context of these dynamic viruses. © 2019 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc- nd/4.0/). Introduction a city-state with a high population density in Southeast Asia, has also been affected by influenza pandemics and epidemics. In Influenza pandemics and seasonal epidemics have resulted in Singapore, Lee et al. (2008) estimated 3500 deaths during the 1918 substantial public health, social and economic impacts. Singapore, A/H1N1 outbreak; 680 deaths and more than 77,000 outpatient attendances during the 1957 A/H2N2 outbreak; and an increase in outpatient attendances of over 65% during the 1968 A/H3N2 * Corresponding authors. outbreak. Cutter et al. (2010) reported 18 A/H1N1-related deaths E-mail addresses: [email protected] (C.K. Kwoh), [email protected] and estimated over 270,000 infected persons during the 2009 (V.T. Chow). outbreak in Singapore. Influenza burden in non-epidemic years has 1 Authors with equal contribution. https://doi.org/10.1016/j.ijid.2019.10.024 1201-9712/© 2019 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). F.X. Ivan et al. / International Journal of Infectious Diseases 90 (2020) 84–96 85 also been assessed. Ng et al. (2002) estimated 630,000 influenza fluid using QIAamp Viral RNA Mini kit (Qiagen, Valencia, CA, USA). cases (>20% of the Singapore population), which gave rise to Viral cDNAs were then generated using SuperScript III reverse 520,000 doctor visits, 315,000 days of sick absence from work, and transcriptase (Invitrogen, Carlsbad, CA, USA) and universal primer about 1,500 deaths among 4,200 infected elderly persons. Ang et al. for influenza A or B (Lee et al., 2013). Reverse transcription (RT) was (2014) estimated that hospitalizations due to influenza were 28– carried out at 50 C for 30 min, followed by enzyme inactivation at 30 per 100,000 person-years during 2004–2008 and 2010–2012, 95 C for 1 min. Subsequently, 40 cycles of polymerase chain with the very young and elderly at higher risk for hospitalization. reaction (PCR) were performed using a T-Personal thermal cycler Overall, these data warrant an effective vaccination program in the (Biometra, Gottingen, Germany) or ABI 2400 thermal cycler population. (Applied Biosystems, Foster City, CA, USA), each consisting of Vaccination targeting particularly the hemagglutinin (HA) has denaturation at 95 C for 15 s, followed by annealing and extension been considered to be a cost-beneficial strategy to reduce influenza at 72 C. One-step qPCR (Lee et al., 2013) was performed to burden (Duncan et al., 2012). Nonetheless, vaccination seems to be differentiate A/H1N1 and A/H3N2 strains, while conventional two- more effective against A/H1N1 and B than against A/H3N2, as step RT-PCR was performed using lineage-specific primers to observed in a study involving Singapore military personnel in 2010– differentiate B/Victoria and B/Yamagata strains. 2013 (Ho et al., 2014). The relative inefficacy of the vaccine against A/ Illumina MiSeq Next Generation Sequencer was employed to H3N2 may be partially explained by the study of Lee et al. (2015), sequence the full genomes of influenza A, while FluSeq v1.0 was whichfound that 84%ofclinicalisolatescollectedin2009–2013were used for genome assembly (Lee et al., 2016). Sanger sequencing mismatched to the vaccine strain A/Perth/16/2009(H3N2) recom- was employed to validate the HA1 segments of influenza A, and to mended by WHO. Interestingly, this study also observed different sequence the genomes of influenza B. A/H3N2 primers (Lee et al., patterns of A/H3N2 dominance in Singapore and regions within the 2013), A/H1N1 primers (Deng et al., 2015) and 18 sets of B primers Northern and Southern hemispheres. This finding highlights the (Tewawong et al., 2015a) were used for sequencing. An additional importance of local or regional vaccine strategy and warrants set of primers (Chi et al., 2005) was also used for sequencing the influenza virus surveillance. Indeed, surveillance studies in HA1 genes of B viruses. The sequence data were analyzed using Singapore have been carried out regularly by the Singapore National MEGA software (Tamura et al., 2013) and the NCBI Influenza Virus Surveillance Program for Influenza that is part of the WHO Sequence Annotation Tool (Bao et al., 2007). international laboratory-based surveillance network (Ang et al., 2016a),inaddition to otherstudiesundervarioussettings(Seahetal., Phylogenetic analyses 2010; Yap et al., 2012; Virk et al., 2017). However, only a few of these surveillance studies were linked to genomic information. For each viral segment of A/H1N1, A/H3N2 and B viruses, a Considering that genomic surveillance may improve vaccine phylogenetic tree was reconstructed
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