Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs

Takemae, Nobuhiro; Ruttanapumma, Ruttapong; Parchariyanon, Sujira; Yoneyama, Shuji; Hayashi, Tsuyoshi; Hiramatsu, Hiroaki; Sriwilaijaroen, Nongluk; Uchida, Yuko; Kondo, Sachiko; Yagi, Hirokazu; Kato, Koichi; Suzuki, Yasuo; Saito, Takehiko

doi:10.1099/vir.0.016691-0

Cited by 44 publications

(36 citation statements)

References 39 publications

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“…Of all HA sequences spanning position 222, close to 92% had 222D, 5.5% had 222E, and 1.4% had 222G, and for 1.3% the amino acid residue at position 222 was uncertain. It has been reported that D222G may arise upon passage of swine influenza A viruses with 222D in embryonated chicken eggs (49). The proportion of sequences with ambiguity at position 222 and sequences with 222G could be related to viral mutants or quasispecies emerging either in vivo or upon propagation in eggs.…”

Section: Discussionmentioning

confidence: 99%

“…However, D222G in HA is of special interest, since it has also been described as the single change in HA between two strains of the "Spanish" 1918 H1N1 virus that differed in receptor specificity (47). Furthermore, upon propagation in embryonated chicken eggs, pdmH1N1 can acquire the mutation rapidly, presumably because it results in virus adaptation to avian (␣2,3-SAs) receptors (49). The presence of the substitution in pdmH1N1s in the human population and its potential association with more severe disease prompted us to test its effect on pdmH1N1 receptor binding, replication, antigenic properties, and pathogenesis and transmission in animal models.…”

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confidence: 99%

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Virulence-Associated Substitution D222G in the Hemagglutinin of 2009 Pandemic Influenza A(H1N1) Virus Affects Receptor Binding

Chutinimitkul

Herfst

Steel

et al. 2010

J Virol

191

210

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The clinical impact of the 2009 pandemic influenza A(H1N1) virus (pdmH1N1) has been relatively low.However, amino acid substitution D222G in the hemagglutinin of pdmH1N1 has been associated with cases of severe disease and fatalities. D222G was introduced in a prototype pdmH1N1 by reverse genetics, and the effect on virus receptor binding, replication, antigenic properties, and pathogenesis and transmission in animal models was investigated. pdmH1N1 with D222G caused ocular disease in mice without further indications of enhanced virulence in mice and ferrets. pdmH1N1 with D222G retained transmissibility via aerosols or respiratory droplets in ferrets and guinea pigs. The virus displayed changes in attachment to human respiratory tissues in vitro, in particular increased binding to macrophages and type II pneumocytes in the alveoli and to tracheal and bronchial submucosal glands. Virus attachment studies further indicated that pdmH1N1 with D222G acquired dual receptor specificity for complex ␣2,3-and ␣2,6-linked sialic acids. Molecular dynamics modeling of the hemagglutinin structure provided an explanation for the retention of ␣2,6 binding. Altered receptor specificity of the virus with D222G thus affected interaction with cells of the human lower respiratory tract, possibly explaining the observed association with enhanced disease in humans.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Virulence-Associated Substitution D222G in the Hemagglutinin of 2009 Pandemic Influenza A(H1N1) Virus Affects Receptor Binding

Chutinimitkul

Herfst

Steel

et al. 2010

J Virol

191

210

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“…Cytokines and chemokines in the BAL fluid of macaques were measured by using the Milliplex MAP nonhuman primate cytokine/chemokine panel (Millipore, Bedford, MA) with the Bio-Plex 200 system (Bio-Rad Laboratories, Hercules, CA). (11,25,29). All test viruses were generated by using reverse genetics (21) and their genomes completely sequenced to rule out unwanted mutations.…”

Section: Cells and Virusesmentioning

confidence: 99%

Avian-Type Receptor-Binding Ability Can Increase Influenza Virus Pathogenicity in Macaques

Watanabe

Shinya

Watanabe

et al. 2011

J Virol

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The first influenza pandemic of the 21st century was caused by novel H1N1 viruses that emerged in early 2009. An Asp-to-Gly change at position 222 of the receptor-binding protein hemagglutinin (HA) correlates with more-severe infections in humans. The amino acid at position 222 of HA contributes to receptor-binding specificity with Asp (typically found in human influenza viruses) and Gly (typically found in avian and classic H1N1 swine influenza viruses), conferring binding to human-and avian-type receptors, respectively. Here, we asked whether binding to avian-type receptors enhances influenza virus pathogenicity. We tested two 2009 pandemic H1N1 viruses possessing HA-222G (isolated from severe cases) and two viruses that possessed HA-222D. In glycan arrays, viruses possessing HA-222D preferentially bound to human-type receptors, while those encoding HA-222G bound to both avian-and human-type receptors. This difference in receptor binding correlated with efficient infection of viruses possessing HA-222G, compared to those possessing HA-222D, in human lung tissue, including alveolar type II pneumocytes, which express avian-type receptors. In a nonhuman primate model, infection with one of the viruses possessing HA-222G caused lung damage more severe than did infection with a virus encoding HA-222D, although these pathological differences were not observed for the other virus pair with either HA-222G or HA-222D. These data demonstrate that the acquisition of avian-type receptor-binding specificity may result in more-efficient infection of human alveolar type II pneumocytes and thus more-severe lung damage. Collectively, these findings suggest a new mechanism by which influenza viruses may become more pathogenic in mammals, including humans.In the early spring of 2009, the human population was confronted by a novel swine origin H1N1 influenza virus that caused the first influenza pandemic of the 21st century. In most cases, human infections with this virus appeared to be mild; however, many severe and fatal cases were reported in individuals who had no other underlying health issues (3). Yet, the virulence factors of the 2009 pandemic H1N1 virus, if any, remain poorly understood.Host range and pathogenicity of influenza viruses are determined by both viral and host factors. The receptor-binding specificity of the hemagglutinin (HA) protein plays a role in host range restriction (18). In general, human influenza viruses preferentially bind to sialic acid linked to galactose by an ␣2,6 linkage (SA␣2,6Gal), which is prevalent in human airway epithelium, whereas avian influenza viruses have higher affinity for SA␣2,3Gal, the major sialyloligosaccharide species in duck intestine, where aquatic bird influenza viruses replicate (24).

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“…For example, human H3N2 clinical specimens can be the source of different sequence variants when propagated in MDCK cells or in embryonated eggs (17). Similarly, classical swine H1N1 viruses isolated in eggs have changes at positions 187 and/or 222 and modulate their receptor specificity (4,18).…”

Section: Discussionmentioning

confidence: 99%

“…Phylogenetic analysis of the 2009 pandemic H1N1 virus (H1N1pdm09) indicated that the genome was a combination of gene segments that had not been previously identified in animal or human influenza viruses (5). The HA gene of H1N1pdm09 belongs to the classical swine lineage distinct from other viruses of human or avian origin that were introduced into pigs more recently, giving rise to 'human-like' and 'avianlike' swine influenza lineages (18). Its ancestry has been traced to the viruses similar to the human pandemic in 1918-1919 (1).…”

Section: Introductionmentioning

confidence: 99%

Substitution in position 222 of haemagglutinin of pandemic influenza A (H1N1) viruses isolated from pigs in Poland

Kowalczyk

Urbaniak

Markowska-Daniel

et al. 2015

Bulletin of the Veterinary Institute in Pulawy

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The aim of the study was to monitor genetic diversity and antigenic changes in the genome of influenza A(H1N1)pdm09 viral isolates detected during the post-pandemic period in Poland. Clinical specimens obtained from three suspected cases of influenza were analysed by sequencing. Among the differences identified in amino acids sequences, nine substitutions were located within the antigenic HA1 sites and in five residues forming receptor-binding pocket. The HA(D222G) mutation was shown in the isolate Swine/Poland/134312/12 obtained from a mild case of the disease. It must be emphasized that, in general, clinically mild cases are caused by the viruses in which that specific mutation, i.e. haemagglutinin (D222G), does not occur.

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Alterations in receptor-binding properties of swine influenza viruses of the H1 subtype after isolation in embryonated chicken eggs

Cited by 44 publications

References 39 publications

Virulence-Associated Substitution D222G in the Hemagglutinin of 2009 Pandemic Influenza A(H1N1) Virus Affects Receptor Binding

Virulence-Associated Substitution D222G in the Hemagglutinin of 2009 Pandemic Influenza A(H1N1) Virus Affects Receptor Binding

Avian-Type Receptor-Binding Ability Can Increase Influenza Virus Pathogenicity in Macaques

Substitution in position 222 of haemagglutinin of pandemic influenza A (H1N1) viruses isolated from pigs in Poland

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