Isolation and Characterization of Influenza C Viruses in the Philippines and Japan

Odagiri, Takashi; Matsuzaki, Yoko; Okamoto, Michiko; Suzuki, Akira; Saito, Mariko; Tamaki, Raita; Lupisan, Socorro; Sombrero, Lydia; Hongō, Seiji; Oshitani, Hitoshi

doi:10.1128/jcm.02628-14

Cited by 22 publications

(27 citation statements)

References 42 publications

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“…Here we described the isolation of a contemporary ICV—C/Victoria/2/2012 (C/Vic)—from a diseased child with acute respiratory symptoms in 2012. Phylogenetic analysis indicated that viral HEF gene was derived from C/Sao Paulo lineage, which is consistent with the finding that the dominant antigenic group is C/Sao Paulo lineage from 2006 to 2016 . However, its most internal genes (PB1, NP, M, and NS) were donated from multiple ICVs.…”

Section: Introductionsupporting

confidence: 86%

Genetic and antigenic characteristics of a human influenza C virus clinical isolate

Liu

Sheng

Lin

et al. 2019

Journal of Medical Virology

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Unlike influenza A and B viruses that infect humans and cause severe diseases in seasonal epidemics, influenza C virus (ICV) is a ubiquitous childhood pathogen typically causing mild respiratory symptoms. ICV infections are rarely diagnosed and less research has been performed on it despite the virus being capable of causing severe disease in infants. Here we report on the isolation of a human ICV from a child with acute respiratory disease, provisionally designated C/Victoria/2/2012 (C/Vic). The full‐length genome sequence and phylogenetic analysis revealed that the hemagglutinin‐esterase‐fusion (HEF) gene of C/Vic was derived from C/Sao Paulo lineage, while its PB2 and P3 genes evolved separately from all characterized historical ICV isolates. Furthermore, antigenic analysis using the hemagglutination inhibition (HI) assay found that 1947 C/Taylor virus (C/Taylor lineage) was antigenically more divergent from1966 C/Johannesburg (C/Aichi lineage) than from 2012 C/Vic. Structure modeling of the HEF protein identified two mutations in the 170‐loop of the HEF protein around the receptor‐binding pocket as a possible antigenic determinant responsible for the discrepant HI results. Taken together, results of our studies reveal novel insights into the genetic and antigenic evolution of ICV and provide a framework for further investigation of its molecular determinants of antigenic property and replication.

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Section: Introductionsupporting

confidence: 86%

Genetic and antigenic characteristics of a human influenza C virus clinical isolate

Liu

Sheng

Lin

et al. 2019

Journal of Medical Virology

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“…Therefore, C/Aichi/1/99 was circulating in Malaysia and had a genome composition distinct from that of C/Yamagata/1/93 (32). The increase in isolates belonging to the C/Sao Paulo lineage in Japan started in 2004 ( the Philippines in 2011 and 2013 had HE genes belonging to the C/Sao Paulo lineage and had the same internal genome composition as C/Miyagi/9/96 (43). Therefore, the viruses isolated in the Philippines are closely related to C/Victoria/2/2012, suggesting that such viruses of the C/Sao Paulo lineage were circulating in Australia and the Philippines in 2011 to 2013 before they spread to Japan.…”

Section: Discussionmentioning

confidence: 99%

Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014

Matsuzaki

Sugawara

Furuse

et al. 2016

J Virol

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Since influenza C virus was first isolated in 1947, the virus has been only occasionally isolated by cell culture; there are only four strains for which complete genome sequences are registered. Here, we analyzed a total of 106 complete genomes, ranging from the first isolate from 1947 to recent isolates from 2014, to determine the genetic lineages of influenza C virus, the reassortment events, and the rates of nucleotide substitution. The results showed that there are six lineages, named C/Taylor, C/Mississippi, C/Aichi, C/Yamagata, C/Kanagawa, and C/Sao Paulo. They contain both antigenic and genetic lineages of the hemagglutininesterase (HE) gene, and the internal genes PB2, PB1, P3, NP, M, and NS are divided into two major lineages, a C/Mississippi/80-related lineage and a C/Yamagata/81-related lineage. Reassortment events were found over the entire period of 68 years. Several outbreaks of influenza C virus between 1990 and 2014 in Japan consisted of reassortant viruses, suggesting that the genomic constellation is related to influenza C virus epidemics. The nucleotide sequences were highly homologous to each other. The minimum percent identity between viruses ranged from 91.1% for the HE gene to 96.1% for the M gene, and the rate of nucleotide substitution for the HE gene was the highest, at 5.20 ؋ 10 ؊4 substitutions/site/year. These results indicate that reassortment is an important factor that increases the genetic diversity of influenza C virus, resulting in its ability to prevail in humans. However, the antigenicity of the HE glycoprotein is highly stable, and antigenic drift has not occurred for at least 30 years. Here, we analyzed a total of 106 complete genomes spanning 68 years for the first time, and we found that influenza C viruses are circulating worldwide while undergoing reassortment as well as selection by herd immunity, resulting in an increased ability to prevail in humans. The results presented in this study contribute to the understanding of the evolution, including reassortment events, underlying influenza C virus epidemics. IMPORTANCE Influenza C virus is a pathogen that causes acute respiratory illness in children and

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“…Isolation of influenza C viruses was performed using Madin–Darby canine kidney (MDCK) cells (ATCC CCL‐34) using maintenance media (DMEM Coon's Basal Media containing sodium bicarbonate (3%) with the addition of 2 mmol/L glutamine, 1% non‐essential amino acids, 0.05% NaHCO3, 0.02 mol/L HEPES, 4% penicillin and streptomycin, 2 μg/mL amphotericin B and 4 μg/mL trypsin). Samples were incubated for up to 5 days at 33°C without CO 2 , and virus growth was quantified by determining the hemagglutination titer (HA) with 0.5% fowl and turkey RBC …”

Section: Methodsmentioning

confidence: 99%

“…A Phylogenetic tree and the bootstrap supports for the HE data set were estimated using the best‐fit evolutionary model and the maximum likelihood (ML) method in PhyML, v3.0, software . Other representative influenza C viruses’ HE sequences were downloaded from GenBank, including the influenza C viruses that make up the antigenically and phylo‐genetically distinct reference groups: C/Taylor/1233.47, C/Aichi/1/81, C/Sao Paulo/378/82, C/Kanagawa/1/76, Yamagata/26/81 and C/Mississippi/80 . Bootstrapping estimates (%) were generated after running 1000 replicates.…”

Section: Methodsmentioning

confidence: 99%

“…2015, who found approximately 10% of children had influenza C present in samples collected from four Japanese hospitals during 2009–2010. Often these cases of influenza C also have other viruses or bacteria detected in the specimen making it difficult to attribute the contribution of influenza C infections to the clinical illness manifestations . In contrast to most viral etiology studies, serological studies often find high seroprevalence rates in the community which rise rapidly up to 10 years of age to around 50%–60% of the population, indicating that widespread transmission has occurred among children in many different countries .…”

Section: Introductionmentioning

confidence: 99%

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Influenza C infections in Western Australia and Victoria from 2008 to 2014

Jelley

Levy

Deng

et al. 2016

Influenza Resp Viruses

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BackgroundInfluenza C is usually considered a minor cause of respiratory illness in humans with many infections being asymptomatic or clinically mild. Large outbreaks can occur periodically resulting in significant morbidity.ObjectivesThis study aimed at analyzing the available influenza C clinical samples from two widely separated states of Australia, collected over a 7‐year period and to compare them with influenza C viruses detected in other parts of the world in recent years.Patients/MethodsBetween 2008 and 2014, 86 respiratory samples that were influenza C positive were collected from subjects with influenza‐like illness living in the states of Victoria and Western Australia. A battery of other respiratory viruses were also tested for in these influenza C‐positive samples. Virus isolation was attempted on all of these clinical samples, and gene sequencing was performed on all influenza C‐positive cultures.Results and conclusionsDetections of influenza C in respiratory samples were sporadic in most years studied, but higher rates of infection occurred in 2012 and 2014. Many of the patients with influenza C had coinfections with other respiratory pathogens. Phylogenetic analysis of the full‐length hemagglutinin–esterase–fusion (HE) gene found that most of the viruses grouped in the C/Sao Paulo/378/82 clade with the remainder grouping in the C/Kanagawa/1/76 clade.

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Isolation and Characterization of Influenza C Viruses in the Philippines and Japan

Cited by 22 publications

References 42 publications

Genetic and antigenic characteristics of a human influenza C virus clinical isolate

Genetic and antigenic characteristics of a human influenza C virus clinical isolate

Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014

Influenza C infections in Western Australia and Victoria from 2008 to 2014

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