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Article: Corrigendum to "Inferring the global phylodynamics of influenza A/H3N2 viruses in Taiwan" [J Formos Med Assoc 118 (2019) 116-124].

Gong, Yu-Nong / Tsao, Kuo-Chien / Chen, Guang-Wu

Journal of the Formosan Medical Association = Taiwan yi zhi

2024 Volume 123, Issue 2, Page(s) 299

Language	English
Publishing date	2024-02-02
Publishing country	Singapore
Document type	Published Erratum
ZDB-ID	2096659-3
ISSN	1876-0821 ; 0929-6646
ISSN (online)	1876-0821
ISSN	0929-6646
DOI	10.1016/j.jfma.2024.01.027
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Article ; Online: Evolution and Epidemiology of SARS-CoV-2 Virus.

Gong, Yu-Nong / Lee, Kuo-Ming / Shih, Shin-Ru

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2452, Page(s) 3–18

Abstract: A novel coronavirus (CoV) that emerged in Wuhan, Hubei province in China, in December 2019, has rapidly spread worldwide. Named as the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), this virus has been responsible for infecting about 153 ... ...

Abstract	A novel coronavirus (CoV) that emerged in Wuhan, Hubei province in China, in December 2019, has rapidly spread worldwide. Named as the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), this virus has been responsible for infecting about 153 million people and causing 3 million deaths by May 2021. There is obvious interest in gaining novel insights into the epidemiologic evolution of this virus; however, inappropriate application and interpretation of genomic and phylogenetic analyses has led to dangerous outcomes and misunderstandings. This chapter focuses on not only introducing this virus, its genomic characteristics and molecular mechanisms but also describing the application and interpretation of phylogenetic tree analyses, in order to provide useful information to better understand the evolution and epidemiology of this virus. In addition, recombinant region and genetic ancestry of SARS-CoV-2 remain unknown. It is urgently required to collect samples and obtain related viral genetic data from animal sources for identifying the intermediate host of SARS-CoV-2 that is responsible for its cross-species transmission.
MeSH term(s)	Animals ; COVID-19/epidemiology ; China/epidemiology ; Humans ; Phylogeny ; SARS-CoV-2/genetics
Language	English
Publishing date	2022-05-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2111-0_1
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Article ; Online: Novel intertypic recombination of Echovirus 11 in the Enterovirus species B.

Gong, Yu-Nong / Yang, Shu-Li / Chen, Yi-Ching / Liu, Yi-Chun / Huang, Yhu-Chering / Tsao, Kuo-Chien

Journal of medical virology

2024 Volume 96, Issue 1, Page(s) e29323

Abstract: Enteroviruses (EVs), single-stranded, positive-sense RNA viruses, can be classified into four species (A-D), which have previously been linked to a diverse range of disease manifestations and infections affecting the central nervous system. In the ... ...

Abstract	Enteroviruses (EVs), single-stranded, positive-sense RNA viruses, can be classified into four species (A-D), which have previously been linked to a diverse range of disease manifestations and infections affecting the central nervous system. In the Enterovirus species B (EV-B), Echovirus type 11 (E11) has been observed to occasionally circulate in Taiwan, which was responsible for an epidemic of enterovirus infections in 2018. Here, 48 clinical specimens isolated in 2003, 2004, 2009, and 2018 were collected for the high-throughput sequencing. Notably, we identified 2018 Taiwanese strains having potential recombinations in the 3D gene, as well as one 2003 strain having a double recombination with E6 and Coxsackievirus B5 in the P2 and P3 regions, respectively. Additionally, one amino acid signature mutated from the Histidine (H) in throat swab specimens to the Tyrosine (Y) in cerebral spinal fluid specimens was detected at position 1496 (or 57) of the genomic coordinate (or 3A gene) to further demonstrate intra-host evolution in different organs. In conclusion, this study identifies potential intertypic recombination events and an intra-host signature mutation in E11 strains, isolated during a 2018 neurological disease outbreak in Taiwan, contributing to our understanding of its evolution and pathogenesis.
MeSH term(s)	Humans ; Phylogeny ; Enterovirus B, Human/genetics ; Enterovirus/genetics ; Enterovirus Infections/epidemiology ; Recombination, Genetic
Language	English
Publishing date	2024-01-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	752392-0
ISSN	1096-9071 ; 0146-6615
ISSN (online)	1096-9071
ISSN	0146-6615
DOI	10.1002/jmv.29323
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Article ; Online: Targeting influenza A virus by splicing inhibitor herboxidiene reveals the importance of subtype-specific signatures around splice sites

Yi-Ju Han / Kuo-Ming Lee / Guan-Hong Wu / Yu-Nong Gong / Avijit Dutta / Shin-Ru Shih

Journal of Biomedical Science, Vol 30, Iss 1, Pp 1-

2023 Volume 22

Abstract: Abstract Background The association between M segment splicing and pathogenicity remains ambiguous in human influenza A viruses. In this study, we aimed to investigate M splicing in various human influenza A viruses and characterize its physiological ... ...

Abstract	Abstract Background The association between M segment splicing and pathogenicity remains ambiguous in human influenza A viruses. In this study, we aimed to investigate M splicing in various human influenza A viruses and characterize its physiological roles by applying the splicing inhibitor, herboxidiene. Methods We examined the M splicing of human H1N1 and H3N2 viruses by comparing three H1N1 and H3N2 strains, respectively, through reverse transcriptase-polymerase chain reaction (RT-PCR) analyses. We randomly selected M sequences of human H1N1, H2N2, and H3N2 viruses isolated from 1933 to 2020 and examined their phylogenetic relationships. Next, we determined the effects of single nucleotide variations on M splicing by generating mutant viruses harboring the 55C/T variant through reverse genetics. To confirm the importance of M2 splicing in the replication of H1N1 and H3N2, we treated infected cells with splicing inhibitor herboxidiene and analyzed the viral growth using plaque assay. To explore the physiological role of the various levels of M2 protein in pathogenicity, we challenged C57BL/6 mice with the H1N1 WSN wild-type strain, mutant H1N1 (55T), and chimeric viruses including H1N1 + H3wt and H1N1 + H3mut. One-tailed paired t-test was used for virus titer calculation and multiple comparisons between groups were performed using two-way analysis of variance. Results M sequence splice site analysis revealed an evolutionarily conserved single nucleotide variant C55T in H3N2, which impaired M2 expression and was accompanied by collinear M1 and mRNA3 production. Aberrant M2 splicing resulted from splice-site selection rather than a general defect in the splicing process. The C55T substitution significantly reduced both M2 mRNA and protein levels regardless of the virus subtype. Consequently, herboxidiene treatment dramatically decreased both the H1N1 and H3N2 virus titers. However, a lower M2 expression only attenuated H1N1 virus replication and in vivo pathogenicity. This attenuated phenotype was restored by M ...
Keywords	Influenza A virus ; Pathogenicity ; Splicing ; Herboxidiene ; Subtype-specific signature ; M2 protein ; Medicine ; R
Subject code	570
Language	English
Publishing date	2023-02-01T00:00:00Z
Publisher	BMC
Document type	Article ; Online
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Article ; Online: Targeting influenza A virus by splicing inhibitor herboxidiene reveals the importance of subtype-specific signatures around splice sites.

Han, Yi-Ju / Lee, Kuo-Ming / Wu, Guan-Hong / Gong, Yu-Nong / Dutta, Avijit / Shih, Shin-Ru

Journal of biomedical science

2023 Volume 30, Issue 1, Page(s) 10

Abstract: Background: The association between M segment splicing and pathogenicity remains ambiguous in human influenza A viruses. In this study, we aimed to investigate M splicing in various human influenza A viruses and characterize its physiological roles by ... ...

Abstract	Background: The association between M segment splicing and pathogenicity remains ambiguous in human influenza A viruses. In this study, we aimed to investigate M splicing in various human influenza A viruses and characterize its physiological roles by applying the splicing inhibitor, herboxidiene. Methods: We examined the M splicing of human H1N1 and H3N2 viruses by comparing three H1N1 and H3N2 strains, respectively, through reverse transcriptase-polymerase chain reaction (RT-PCR) analyses. We randomly selected M sequences of human H1N1, H2N2, and H3N2 viruses isolated from 1933 to 2020 and examined their phylogenetic relationships. Next, we determined the effects of single nucleotide variations on M splicing by generating mutant viruses harboring the 55C/T variant through reverse genetics. To confirm the importance of M2 splicing in the replication of H1N1 and H3N2, we treated infected cells with splicing inhibitor herboxidiene and analyzed the viral growth using plaque assay. To explore the physiological role of the various levels of M2 protein in pathogenicity, we challenged C57BL/6 mice with the H1N1 WSN wild-type strain, mutant H1N1 (55T), and chimeric viruses including H1N1 + H3wt and H1N1 + H3mut. One-tailed paired t-test was used for virus titer calculation and multiple comparisons between groups were performed using two-way analysis of variance. Results: M sequence splice site analysis revealed an evolutionarily conserved single nucleotide variant C55T in H3N2, which impaired M2 expression and was accompanied by collinear M1 and mRNA3 production. Aberrant M2 splicing resulted from splice-site selection rather than a general defect in the splicing process. The C55T substitution significantly reduced both M2 mRNA and protein levels regardless of the virus subtype. Consequently, herboxidiene treatment dramatically decreased both the H1N1 and H3N2 virus titers. However, a lower M2 expression only attenuated H1N1 virus replication and in vivo pathogenicity. This attenuated phenotype was restored by M replacement of H3N2 M in a chimeric H1N1 virus, despite low M2 levels. Conclusions: The discrepancy in M2-dependence emphasizes the importance of M2 in human influenza A virus pathogenicity, which leads to subtype-specific evolution. Our findings provide insights into virus adaptation processes in humans and highlights splicing regulation as a potential antiviral target.
MeSH term(s)	Animals ; Mice ; Humans ; Influenza A virus/genetics ; Influenza A Virus, H1N1 Subtype/genetics ; Influenza A Virus, H3N2 Subtype/genetics ; Phylogeny ; Mice, Inbred C57BL ; Nucleotides ; Influenza, Human/drug therapy ; Influenza, Human/genetics
Chemical Substances	herboxidiene (142861-00-5) ; Nucleotides
Language	English
Publishing date	2023-02-03
Publishing country	England
Document type	Journal Article
ZDB-ID	1193378-1
ISSN	1423-0127 ; 1021-7770
ISSN (online)	1423-0127
ISSN	1021-7770
DOI	10.1186/s12929-023-00897-4
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Zs.A 4037: Show issues

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Article ; Online: Methods for detection and study of virus-derived small RNAs produced from the intramolecular base-pairing region of the picornavirus genome.

Lee, Kuo-Ming / Gong, Yu-Nong / Shih, Shin-Ru

Methods (San Diego, Calif.)

2019 Volume 183, Page(s) 4–12

Abstract: There is conclusive evidential support for the existence of virus-derived small RNA (vsRNA) in mammals. Two types of vsRNA have been reported from picornaviruses. The first is virus-derived short-interfering RNA (vsiRNA) that is processed from viral ... ...

Abstract	There is conclusive evidential support for the existence of virus-derived small RNA (vsRNA) in mammals. Two types of vsRNA have been reported from picornaviruses. The first is virus-derived short-interfering RNA (vsiRNA) that is processed from viral double-stranded RNA intermediates during RNA replication. The other is small RNA derived from the highly base-paired single-stranded genomic region, e.g. the internal ribosome entry site (IRES) of picornaviruses. vsiRNA interacts with the Argonaute protein to control viral RNA replication through the process of RNA interference. However, the function of structure-based vsRNA is largely unknown. We previously identified vsRNA1 generated from the enterovirus-A71 (EV-A71) IRES region by the endogenous enzyme Dicer. Exogenous vsRNA1 can inhibit IRES activity both in vivo and in vitro, hence viral replication is inhibited. Here we describe key methods used to characterize vsRNA, including annotation by next-generation sequencing, abundance measurement by Northern blotting, determination of Dicer-dependence by gel-shift assay and in vitro cleavage assay, and the inhibitory effect on IRES activity via in vitro translation assay.
MeSH term(s)	Animals ; Blotting, Northern/methods ; Cell Line, Tumor ; DEAD-box RNA Helicases ; Electrophoresis, Polyacrylamide Gel/methods ; Electrophoretic Mobility Shift Assay/methods ; Enterovirus A, Human/genetics ; Gene Expression Regulation, Viral ; Genome, Viral ; Humans ; Internal Ribosome Entry Sites/genetics ; Mice ; RNA Interference ; RNA, Small Interfering ; RNA, Viral/analysis ; RNA, Viral/metabolism ; Ribonuclease III ; Sequence Analysis, RNA/methods ; Virus Replication/genetics
Chemical Substances	Internal Ribosome Entry Sites ; RNA, Small Interfering ; RNA, Viral ; DICER1 protein, human (EC 3.1.26.3) ; Ribonuclease III (EC 3.1.26.3) ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2019-09-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1066584-5
ISSN	1095-9130 ; 1046-2023
ISSN (online)	1095-9130
ISSN	1046-2023
DOI	10.1016/j.ymeth.2019.08.011
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Article: Visualizing Influenza A Virus vRNA Replication.

Chiu, Ya-Fang / Huang, Yi-Wen / Chen, Chi-Yuan / Chen, Yu-Chia / Gong, Yu-Nong / Kuo, Rei-Lin / Huang, Chung-Guei / Shih, Shin-Ru

Frontiers in microbiology

2022 Volume 13, Page(s) 812711

Abstract: Influenza A virus (IAV) has caused recurrent epidemics and severe pandemics. In this study, we adapted an MS2-MCP live-cell imaging system to visualize IAV replication. A reporter plasmid, pHH-PB2-vMSL, was constructed by replacing a part of the PB2- ... ...

Abstract	Influenza A virus (IAV) has caused recurrent epidemics and severe pandemics. In this study, we adapted an MS2-MCP live-cell imaging system to visualize IAV replication. A reporter plasmid, pHH-PB2-vMSL, was constructed by replacing a part of the PB2-coding sequence in pHH-PB2 with a sequence encoding 24 copies of a stem-loop structure from bacteriophage MS2 (MSL). Binding of MS2 coat protein (MCP) fused to green fluorescent protein (GFP) to MSL enabled the detection of vRNA as fluorescent punctate signals in live-cell imaging. The introduction of pHH-PB2-vMSL into A549 cells transduced to express an MCP-GFP fusion protein lacking the nuclear localization signal (MCP-GFPdN), subsequently allowed tracking of the distribution and replication of PB2-vMSL vRNA after IAV PR8 infection. Spatial and temporal measurements revealed exponential increases in vRNA punctate signal intensity, which was only observed after membrane blebbing in apoptotic cells. Similar signal intensity increases in apoptotic cells were also observed after MDCK cells, transduced to express MCP-GFPdN, were infected with IAV carrying PB2-vMSL vRNA. Notably, PB2-vMSL vRNA replication was observed to occur only in apoptotic cells, at a consistent time after apoptosis initiation. There was a lack of observable PB2-vMSL vRNA replication in non-apoptotic cells, and vRNA replication was suppressed in the presence of apoptosis inhibitors. These findings point to an important role for apoptosis in IAV vRNA replication. The utility of the MS2-imaging system for visualizing time-sensitive processes such as viral replication in live host cells is also demonstrated in this study.
Language	English
Publishing date	2022-06-06
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2022.812711
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Article ; Online: Inferring the global phylodynamics of influenza A/H3N2 viruses in Taiwan

Yu-Nong Gong / Kuo-Chien Tsao / Guang-Wu Chen

Journal of the Formosan Medical Association, Vol 118, Iss 1, Pp 116-

2019 Volume 124

Abstract: Background/Purpose: Influenza A/H3N2 viruses are characterized by highly mutated RNA genomes. In this study, we focused on tracing the phylodynamics of Taiwanese strains over the past four decades. Methods: All Taiwanese H3N2 HA1 sequences and references ...

Abstract	Background/Purpose: Influenza A/H3N2 viruses are characterized by highly mutated RNA genomes. In this study, we focused on tracing the phylodynamics of Taiwanese strains over the past four decades. Methods: All Taiwanese H3N2 HA1 sequences and references were downloaded from public database. A Bayesian skyline plot (BSP) and phylogenetic tree were used to analyze the evolutionary history, and Bayesian phylogeographic analysis was applied to predict the spatiotemporal migrations of influenza outbreaks. Results: Genetic diversity was found to have peaked near the summer of 2009 in BSP, in addition to the two earlier reported ones in summer of 2005 and 2007. We predicted their spatiotemporal migrations and found the summer epidemic of 2005 from Korea, and 2007 and 2009 from the Western United States. BSP also predicted an elevated genetic diversity in 2015–2017. Quasispecies were found over approximately 20% of the strains included in this time span. In addition, a first-time seen N31S mutation was noted in Taiwan in 2016–2017. Conclusion: We comprehensively investigated the evolutionary history of Taiwanese strains in 1979–2017. An epidemic caution could thus be raised if genetic diversity was found to have peaked. An example showed a newly-discovered cluster in 2016–2017 strains featuring a mutation N31S together with HA-160 quasispecies. Phylogeographic analysis, moreover, provided useful insights in tracing the possible source and migrations of these epidemics around the world. We demonstrated that Asian destinations including Taiwan were the immediate followers, while U.S. continent was predicted the origin of two summer epidemics in 2007 and 2009. Keywords: Influenza A/H3N2 viruses, Phylodynamics, Phylogeography, Summer epidemics, Viral quasispecies
Keywords	Medicine (General) ; R5-920
Language	English
Publishing date	2019-01-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article: Inferring the global phylodynamics of influenza A/H3N2 viruses in Taiwan.

Gong, Yu-Nong / Tsao, Kuo-Chien / Chen, Guang-Wu

Journal of the Formosan Medical Association = Taiwan yi zhi

2018 Volume 118, Issue 1 Pt 1, Page(s) 116–124

Abstract: Background/purpose: Influenza A/H3N2 viruses are characterized by highly mutated RNA genomes. In this study, we focused on tracing the phylodynamics of Taiwanese strains over the past four decades.: Methods: All Taiwanese H3N2 HA1 sequences and ... ...

Abstract	Background/purpose: Influenza A/H3N2 viruses are characterized by highly mutated RNA genomes. In this study, we focused on tracing the phylodynamics of Taiwanese strains over the past four decades. Methods: All Taiwanese H3N2 HA1 sequences and references were downloaded from public database. A Bayesian skyline plot (BSP) and phylogenetic tree were used to analyze the evolutionary history, and Bayesian phylogeographic analysis was applied to predict the spatiotemporal migrations of influenza outbreaks. Results: Genetic diversity was found to have peaked near the summer of 2009 in BSP, in addition to the two earlier reported ones in summer of 2005 and 2007. We predicted their spatiotemporal migrations and found the summer epidemic of 2005 from Korea, and 2007 and 2009 from the Western United States. BSP also predicted an elevated genetic diversity in 2015-2017. Quasispecies were found over approximately 20% of the strains included in this time span. In addition, a first-time seen N31S mutation was noted in Taiwan in 2016-2017. Conclusion: We comprehensively investigated the evolutionary history of Taiwanese strains in 1979-2017. An epidemic caution could thus be raised if genetic diversity was found to have peaked. An example showed a newly-discovered cluster in 2016-2017 strains featuring a mutation N31S together with HA-160 quasispecies. Phylogeographic analysis, moreover, provided useful insights in tracing the possible source and migrations of these epidemics around the world. We demonstrated that Asian destinations including Taiwan were the immediate followers, while U.S. continent was predicted the origin of two summer epidemics in 2007 and 2009.
MeSH term(s)	Bayes Theorem ; Forecasting ; Hemagglutinin Glycoproteins, Influenza Virus/genetics ; Humans ; Influenza A Virus, H3N2 Subtype/genetics ; Influenza, Human/epidemiology ; Influenza, Human/virology ; Phylogeny ; Phylogeography ; Risk Factors ; Seasons ; Taiwan/epidemiology
Chemical Substances	Hemagglutinin Glycoproteins, Influenza Virus
Language	English
Publishing date	2018-02-21
Publishing country	Singapore
Document type	Journal Article
ZDB-ID	2096659-3
ISSN	1876-0821 ; 0929-6646
ISSN (online)	1876-0821
ISSN	0929-6646
DOI	10.1016/j.jfma.2018.01.019
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Article: Evolution of Influenza A(H3N2) Viruses in 2 Consecutive Seasons of Genomic Surveillance, 2021-2023.

Fall, Amary / Han, Lijie / Yunker, Madeline / Gong, Yu-Nong / Li, Tai-Jung / Norton, Julie M / Abdullah, Omar / Rothman, Richard E / Fenstermacher, Katherine Z J / Morris, C Paul / Pekosz, Andrew / Klein, Eili / Mostafa, Heba H

Open forum infectious diseases

2023 Volume 10, Issue 12, Page(s) ofad577

Abstract: Background: The circulation and the genomic evolution of influenza A(H3N2) viruses during the 2021/2022 and 2022/2023 seasons were studied and associated with infection outcomes.: Methods: Remnant influenza A-positive samples following standard-of- ... ...

Abstract	Background: The circulation and the genomic evolution of influenza A(H3N2) viruses during the 2021/2022 and 2022/2023 seasons were studied and associated with infection outcomes. Methods: Remnant influenza A-positive samples following standard-of-care testing from patients across the Johns Hopkins Health System (JHHS) were used for the study. Samples were randomly selected for whole viral genome sequencing. The sequence-based pEpitope model was used to estimate the predicted vaccine efficacy (pVE) for circulating H3N2 viruses. Clinical data were collected and associated with viral genomic data. Results: A total of 121 683 respiratory specimens were tested for influenza at JHHS between 1 September 2021 and 31 December 2022. Among them, 6071 (4.99%) tested positive for influenza A. Of these, 805 samples were randomly selected for sequencing, with hemagglutinin (HA) segments characterized for 610 samples. Among the characterized samples, 581 were H3N2 (95.2%). Phylogenetic analysis of HA segments revealed the exclusive circulation of H3N2 viruses with HA segments of the 3C.2a1b.2a.2 clade. Analysis of a total of 445 complete H3N2 genomes revealed reassortments; 200 of 227 of the 2022/2023 season genomes (88.1%) were found to have reassorted with clade 3C.2a1b.1a. The pVE was estimated to be -42.53% for the 2021/2022 season and 30.27% for the 2022/2023 season. No differences in clinical presentations or admissions were observed between the 2 seasons. Conclusions: The increased numbers of cases and genomic diversity of influenza A(H3N2) during the 2022/2023 season were not associated with a change in disease severity compared to the previous influenza season.
Language	English
Publishing date	2023-11-16
Publishing country	United States
Document type	Journal Article
ZDB-ID	2757767-3
ISSN	2328-8957
ISSN	2328-8957
DOI	10.1093/ofid/ofad577
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