Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray

Childs, Robert A.; Palma, Angelina S.; Wharton, Steve; Matrosovich, Tatyana; Liu, Yan; Chai, Wengang; Campanero-Rhodes, María Asunción; Zhang, Yibing; Eickmann, Markus; Kiso, Makoto; Hay, Alan J.; Matrosovich, Mikhail; Feizi, Ten

doi:10.1038/nbt0909-797

Cited by 303 publications

(281 citation statements)

References 19 publications

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“…31 It was shown in vitro that the 2009 H1N1 virus binds to both SAa2-6Gal and SAa2-3Gal. 32 In this study, cases 1-4 presented with DAD with InfA-NP-positive pneumocytes. We expected to find the D222G substitution in hemagglutinin gene recovered from lung specimens in these cases, but it was only detected in case 1.…”

Section: Discussionmentioning

confidence: 56%

Histopathological and immunohistochemical findings of 20 autopsy cases with 2009 H1N1 virus infection

et al. 2012

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, were histopathologically analyzed. Hematoxylin-eosin staining, immunohistochemistry for type A influenza nucleoprotein antigen, and real-time reverse transcription-PCR assay for viral RNA were performed on formalin-fixed and paraffin-embedded specimens. In addition, the D222G amino acid substitution in influenza virus hemagglutinin, which binds to specific cell receptors, was analyzed in formalinfixed and paraffin-embedded trachea and lung sections by direct sequencing of PCR-amplified products. There were several histopathological patterns in the lung according to the most remarkable findings in each case: acute diffuse alveolar damage (DAD) with a hyaline membrane (four cases), organized DAD (one case), acute massive intra-alveolar edema with variable degrees of hemorrhage (three cases), neutrophilic bronchopneumonia (five cases) and tracheobronchitis with limited histopathological changes in alveoli (four cases). In two cases, the main findings were due to preexisting disease. Influenza virus antigen was only detected in the respiratory tract in 10 cases by immunohistochemistry. The antigen was detected in type II pneumocytes (three cases) in the epithelial cells of the trachea, bronchi and glands (six cases), and in the epithelial cells in both of the above (one case). The four cases with acute DAD presented with antigen-positive type II pneumocytes. In one case, the D222G substitution was detected in the lung as a major sequence, although 222D was prominent in the trachea, suggesting that selection of the viral clones occurred in the respiratory tract. In five

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Section: Discussionmentioning

confidence: 56%

Histopathological and immunohistochemical findings of 20 autopsy cases with 2009 H1N1 virus infection

et al. 2012

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“…The CT-Sw/1204 virus also became virulent in BALB/c mice known to express predominantly α2,3-sialic acid in their lungs (24), and demonstrated enhanced infectivity and growth in human lung tissues, indicating potentially productive pulmonary replication. Notably, severe viral pneumonia attributed to efficient virus attachment to α2,3-sialic acid glycoconjugates deep in the lungs have been observed in H5N1 (25) and HA 225G variants of the pH1N1 (5,(26)(27)(28)(29)(30) virus infections. Moreover, it has been demonstrated that avian-type receptor-binding ability because of HA 225G increased pathogenicity of the pH1N1 2009 virus in nonhuman primates (31).…”

Section: Discussionmentioning

confidence: 99%

“…The pH1N1 virus uniquely comprises segments from North American-like triple-reassortant swine (TRSw) H1 viruses (six genes) and Eurasian avian-like swine viruses [neuraminidase (NA) and matrix genes] (3,4). Although most pH1N1 infections were mild, the virus was highly transmissible and could replicate deep in the lungs (5). Introduction of known virulence factors into the pH1N1 virus did not significantly alter its disease phenotype (6,7), suggesting the presence of unknown molecular determinants of pathogenicity and transmissibility.…”

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confidence: 99%

Virulence and transmissibility of H1N2 influenza virus in ferrets imply the continuing threat of triple-reassortant swine viruses

Pascua

Song

Lee

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Efficient worldwide swine surveillance for influenza A viruses is urgently needed; the emergence of a novel reassortant pandemic H1N1 (pH1N1) virus in 2009 demonstrated that swine can be the direct source of pandemic influenza and that the pandemic potential of viruses prevalent in swine populations must be monitored. We used the ferret model to assess the pathogenicity and transmissibility of predominant Korean triple-reassortant swine (TRSw) H1N2 and H3N2 influenza viruses genetically related to North American strains. Although most of the TRSw viruses were moderately pathogenic, one [A/Swine/Korea/1204/2009; Sw/1204 (H1N2)] was virulent in ferrets, causing death within 10 d of inoculation, and was efficiently transmitted to naive contact ferrets via respiratory droplets. Although molecular analysis did not reveal known virulence markers, the Sw/1204 virus acquired mutations in hemagglutinin (HA) (Asp-225-Gly) and neuraminidase (NA) (Ser-315-Asn) proteins during the single ferret passage. The contact-Sw/1204 virus became more virulent in mice, replicated efficiently in vitro, extensively infected human lung tissues ex vivo, and maintained its ability to replicate and transmit in swine. Reverse-genetics studies further indicated that the HA 225G and NA 315N substitutions contributed substantially in altering virulence and transmissibility. These findings support the continuing threat of some field TRSw viruses to human and animal health, reviving concerns on the capacity of pigs to create future pandemic viruses. Apart from warranting continued and enhanced global surveillance, this study also provides evidence on the emerging roles of HA 225G and NA 315N as potential virulence markers in mammals.

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“…However, there are far fewer studies of the receptor selectivity determinants of influenza B virus HA (Suzuki et al, 1992;Matrosovich et al, 1993;Gambaryan et al, 1997Gambaryan et al, , 1999Wang et al, 2007). The importance of developing simple method for typing HA receptor-binding selectivity was heightened by the recent outbreak of swine-origin influenza strains in humans such as the pandemic influenza A 2009 H1N1 virus (Childs et al, 2009;Itoh et al, 2009;Maines et al, 2009). Currently available receptor-characterizing assays include nuclear magnetic resonance, glycan array screening, surface plasmon resonance, hemagglutination or HA inhibition tests, thin-layer chromatography, and ELISA (Rogers and Paulson, 1983;Sauter et al, 1989;Gambaryan and Matrosovich, 1992;Suzuki et al, 1992;Takemoto et al, 1996;Alvarez and Blixt, 2006;Stevens et al, 2006a;Szretter et al, 2006;Hidari et al, 2007;Chandrasekaran et al, 2008;Mandenius et al, 2008;Srinivasan et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…HA of avian influenza viruses usually display a preference for α2-3-linked sialyl-glycans, whereas HA of human influenza viruses preferentially bind α2-6-linked sialyl-glycans (Skehel and Wiley, 2000;Gamblin et al, 2004;Suzuki, 2005;Stevens et al, 2006b). Human influenza B and swine influenza A viruses have been reported to bind both α2,3 and α2,6-linked sialyl-glycans (Ito et al, 1998;Gamblin et al, 2004;Wang et al, 2007;Childs et al, 2009;Maines et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

A gel-capture assay for characterizing the sialyl-glycan selectivity of influenza viruses

Velkov¹,

Thompson²,

El‐Kabbani³

et al. 2011

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Summary. -Sialic acids (SA) usually linked to galactose (Gal) in an α2,6-or α2,3-configuration are considered the main cell receptors for influenza viruses, in particular for their hemagglutinins (HA). The typing of influenza virus HA receptor selectivity is relevant for understanding the transmissibility of avian and swine viruses to the human population. In this study we developed a simple and inexpensive gel-capture assay (GCA) of the influenza virus HA receptor-binding selectivity. Its principle is the binding of soluble influenza virus to pentasaccharide analogs, representatives of receptors of human and avian influenza viruses, immobilized on a gel resin. The human and avian analogs consisted of a sialyllactose-N-tetraose c (LSTc) [Neu5Ac(α2,6)Gal(β1-3) GlcNAc(β1-3)Gal(β1-4)Glc] and a sialyllactose-N-tetraose a (LSTa) [Neu5Ac(α2,3)Gal(β1-3)GlcNAc(β1-3) Gal(β1-4)Glc], respectively. Following equilibration, the unbound virus is washed away and the bound one is assayed via HA by densitometry as a function of the analog concentration. Using GCA, the receptor selectivity of three influenza viruses of different HA subtype was investigated. The results showed that the egg-adapted A/California/07/2009 (H1N1) virus exhibited an avian α2,3-linked LSTa selectivity, however, it retained the ability to bind to the α2,6-linked LSTc human receptor analog. Influenza B virus B/Florida/4/2006 showed α2,6-linked LSTc selectivity and a poor α2,3-linked LSTa avidity. The H3N2 virus A/Wisconsin/15/2009 displayed almost comparable avidity for both receptor analogs with a marginally greater α2,3-linked LSTa avidity. The described assay protocol provides a simple and rapid method for the characterization of influenza virus HA receptor binding selectivity. Keywords: influenza virus; hemagglutinin; receptor; sialyllactose-N-tetraose; gel-capture assay * Corresponding authors. E-mail: Tony.Velkov@monash.edu.au, Steve.Rockman@csl.com.au ; fax: +61-3-9903 9582. Abbreviations: 3ʹSL = 3ʹ-sialyl(N-acetyllactose); 6ʹSLN = 6ʹ-sialyl(Nacetyllactosamine); BPL = β-propiolactone; GCA = gel-capture assay; HA = hemagglutinin; LSTa = sialyllactose-N-tetraose a; LSTc = sialyllactose-N-tetraose c; SA = sialic acids

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Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray

Cited by 303 publications

References 19 publications

Histopathological and immunohistochemical findings of 20 autopsy cases with 2009 H1N1 virus infection

Histopathological and immunohistochemical findings of 20 autopsy cases with 2009 H1N1 virus infection

Virulence and transmissibility of H1N2 influenza virus in ferrets imply the continuing threat of triple-reassortant swine viruses

A gel-capture assay for characterizing the sialyl-glycan selectivity of influenza viruses

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