Evolution of the haemagglutinin-esterase gene of influenza C virus

Muraki, Yasushi; Hongō, Seiji; Sugawara, Kanetsu; Kitame, Fumio; Nakamura, Kenzo

doi:10.1099/0022-1317-77-4-673

Cited by 41 publications

(46 citation statements)

References 27 publications

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“…These observations suggest that the production of antigenic variants by immune selection has not occurred for the last 3 decades. This finding is well comparable with our previous indication that HE protein might no longer be able to evolve in response to antibody pressure because of a high degree of functional constraint on the change of its immunodominant region, which is near the receptor-binding site (15,21). On the other hand, as shown in Fig.…”

Section: Discussionsupporting

confidence: 81%

“…In order to confirm the results of the antigenic analysis, the sequence of the HE gene (nucleotide 64 to 1,989) was determined for 12 strains (Table 2) and a phylogenetic tree was constructed by using them in addition to the 62 published sequences (1,3,4,12,16,17,18,19,21,22,24,25,26,27,33) as well as the sequences of two old strains (YA186 and SHI79) determined here.…”

Section: Resultsmentioning

confidence: 99%

“…Antigenic variation exists among influenza C virus isolates, as demonstrated clearly by antigenic analysis with anti-HE monoclonal antibodies (MAbs) (1,12,16,18,29). Nevertheless, analysis with polyclonal immune sera showed a high degree of cross-reaction among all the isolates examined so far (6,11,16,18,21), indicating that influenza C virus is antigenically much more stable than human influenza A virus. The significance of antigenic variation in influenza C virus epidemiology remains to be clarified.…”

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confidence: 99%

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Frequent Reassortment among Influenza C Viruses

Matsuzaki

Mizuta²,

Sugawara

et al. 2003

J Virol

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126

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In a 9-year survey from December 1990 to December 1999 in Sendai City, Japan, we succeeded in isolating a total of 45 strains of influenza C virus. These 45 strains were isolated in clusters within 4 months in a year, especially from winter to early summer. Previous studies of the hemagglutinin-esterase genes of various influenza C virus isolates revealed the existence of five distinct virus lineages (Aichi/1/81-, Yamagata/26/81-, Mississippi/80-, Sao Paulo/82-, and Kanagawa/1/76-related lineage) in Japan between 1970 and the early 1990s

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Section: Discussionsupporting

confidence: 81%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Frequent Reassortment among Influenza C Viruses

Matsuzaki

Mizuta²,

Sugawara

et al. 2003

J Virol

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126

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“…In order to confirm the results of the antigenic analysis, which suggested that all the 1996 and 1998 isolates from Yamagata City have HE genes belonging to the YA2681-related lineage, the sequence of the HE gene (nucleotides 64 to 1989) was determined for 7 ( 33 isolates, and a phylogenetic tree was constructed by using these 7 sequences in addition to the 42 published sequences (1,3,4,13,15,16,17,20,21,25,26,27,28,33) as well as the 12 sequences of the 1993 to 1996 isolates from Sendai City determined here (see below for details). …”

Section: Resultsmentioning

confidence: 99%

Antigenic and Genetic Characterization of Influenza C Viruses Which Caused Two Outbreaks in Yamagata City, Japan, in 1996 and 1998

Matsuzaki

Sugawara

Mizuta³

et al. 2002

J Clin Microbiol

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, a total of 33 strains of influenza C virus were isolated from 10,726 throat swab specimens collected from children with acute respiratory illness who visited two pediatric clinics in Yamagata City, Japan. These 33 strains were isolated in clusters during two different periods, 20 strains in May to August 1996 and the remaining 13 in March to June 1998. Antigenic analysis with monoclonal antibodies to the hemagglutinin-esterase (HE) glycoprotein and phylogenetic analysis of seven RNA segments showed that the 33 influenza C viruses isolated were antigenically and genetically similar and that they were reassortant viruses which had obtained PB2, PB1, HE, M, and NS genes from a C/pig/Beijing/ 115/81-like virus and P3 and NP genes from a C/Mississippi/80-like virus. These observations suggest strongly that during the survey period of 3 years, two outbreaks of influenza C occurred in Yamagata City, both of which were caused by a reassortant virus having the genome composition described above.Influenza C virus usually causes a mild upper respiratory illness (11) but can also cause lower respiratory infections, such as bronchitis and pneumonia (19). Although seroepidemiological studies revealed that influenza C virus is widely distributed throughout the world (5, 9, 10, 22), outbreaks of illness caused by the virus have rarely been detected, and the virus has been isolated only occasionally (6,7,8,11,12,18). Therefore, information about the epidemiology of influenza C is scarce compared to that for influenza A and influenza B.The genome of the influenza C virus consists of seven RNA segments, which encode three polymerase proteins (PB2, PB1, and P3), hemagglutinin-esterase (HE) glycoprotein, nucleoprotein (NP), matrix (M1) protein, and two nonstructural proteins (NS1 and NS2) (reviewed in reference (14). Thus, reassortment characterized by exchange of genome segments between two different influenza C virus strains occurs not only in vitro (24) but also in nature (2,17,27,32). However, the epidemiological significance of genetic reassortment in influenza C viruses is unknown.To obtain more information about influenza C epidemiology, we developed a tissue culture method for primary virus isolation that is convenient for routine work with a large number of specimens (19, 23) and then initiated surveillance for influenza C virus infections in Yamagata City in 1988 and in the adjacent city of Sendai in 1990. We compared the antigenic specificity of the HE glycoprotein as well as the HE gene sequence among 42 strains isolated between 1947 and 1993 (which included 13 strains obtained by our surveillance work) and revealed the existence of six distinct virus groups, represented by strains Taylor/47, Kanagawa/1/76 (KA176), Yamagata/26/81 (YA2681), Aichi/1/81 (AI181), Sao Paulo/378/82 (SP82), and Mississippi/80 (MS80), four of which (YA2681-, AI181-, SP82-, and MS80-related lineages) circulated in Japan in the 1980s and the early 1990s (17).We report here the results of a 3-year survey (January 1996 to December 1998) performed ...

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“…Szczepy ICV izolowane od ludzi reprezentują jeden podtyp, wykazują niski poziom zmienności genetycznej i ewoluują około dziewięciokrotnie wolniej niż IAV. Do chwili obecnej wyodrębniono sześć linii genetycznych ludzkich szczepów ICV o wysokim pokrewieństwie (> 95%) (17,23). Podobnie jak IBV, ICV nie powodują pandemii grypy (7).…”

Section: Wirusy Grypy Typu Bunclassified

Characterization of a new influenza virus type D

Markowska-Daniel¹,

Mickiewicz²,

Witkowski³

et al. 2016

Medycyna Weterynaryjna

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Influenza is caused by viruses belonging to the Orthomyxoviridae family. Currently three types of influenza virus are known: A (Influenza A virus, IAV), B (IBV) and C (ICV). Despite the fact that all these viruses are derived from a common ancestor they differ from each other by the number of segments, the size and sequence of RNA segments, antigenicity, pathogenicity and the spectrum of natural reservoirs. In 2011, a new influenza virus was isolated in the USA from pigs manifesting influenza-like symptoms. The virus was the most closely related to ICV. It was able to replicate in vitro in different cell cultures and displayed much broader cell tropism than human ICV. Moreover, in contrast to ICV, it was able to replicate at 370C. Electron microscopic studies demonstrated features characteristic of Orthomyxoviruses. Despite morphological and organizational similarities, the biological properties of the new virus, including biochemical activity, differ from that of other influenza viruses. Enzymatic assays revealed that the new virus had negligible neuraminidase but detectable O-acetyloesterase activity. Further studies evidenced that the new virus varied from ICV in receptor binding, despite its sharing a conserved array of functional domains in the viral RNA genome replication and viral entry machinery. Analysis conducted with the use of the model of crystal structure of the hemagglutinin-esterase fusion protein (HE) of the new virus and its receptor demonstrated that this protein was multifunctional. It catalyzes cellular receptor binding, receptor cleavage, as well as membrane fusion. Moreover, divergent receptor-binding sites than HE of ICV have been discovered in the new virus. These amino acid differences may alter the binding specificity and affinity of the HE protein to the receptor that in turn result in the observed differences in cellular tropism between the two viruses. It also possesses an open channel between the 230-helix and 270-loop in the receptor-binding site, which is a unique feature of this virus. This might explain why the new virus has a broad cell tropism. It is possible that the sequence variation in the fusion domain may influence the replication of this virus at a higher temperature when compared to ICV. Next-generation sequencing demonstrated that the genome of the new virus, similarly to ICV, had seven single-stranded negative-sense RNA segments coding 9 viral proteins. Deep RNA sequencing found a M1 protein expression strategy different from that of ICV. Studies aimed at evaluating of the evolutionary relationship of both viruses revealed that the new virus and ICV shared an approximately 69-72% mean pairwise identity in the PB1 gene, which is reported to be the most conserved influenza virus protein. Additionally, differences were detected at 5’ and 3’ends of noncoding regions, which are also highly conserved. They both may be responsible for the lack of in vitro reassortment between ICV of human origin and the new virus. In the study characterizing antigenic properties of the new virus, no cross-reactivity was observed using HI and AGID tests. This indicates the major differences in conserved proteins M1 and NP between both viruses. Summing up, despite the fact that new virus is the most closely related to human ICV, the number of important antigenic and genetic distinctions among them is the basis for suggesting that the International Committee of Virus Taxonomy classify it as a separate genus - D. There is no doubt that the discovery of a new influenza virus genus will have a great impact on influenza research and ecology.

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Evolution of the haemagglutinin-esterase gene of influenza C virus

Cited by 41 publications

References 27 publications

Frequent Reassortment among Influenza C Viruses

Frequent Reassortment among Influenza C Viruses

Antigenic and Genetic Characterization of Influenza C Viruses Which Caused Two Outbreaks in Yamagata City, Japan, in 1996 and 1998

Characterization of a new influenza virus type D

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