Antigenic Characterization of H3 Subtypes of Avian Influenza A Viruses from North America

Bailey, Elizabeth J.; Liang, Liping; Zhao, Nan; Hall, Jeffrey S.; Baroch, John A.; Nolting, Jacqueline M.; Senter, Lucy H.; Cunningham, Frederick L.; Pharr, G. T.; Hanson, Larry A.; Slemons, Richard D.; DeLiberto, Thomas J.; Wan, Xiu‐Feng

doi:10.1637/11086-041015-regr

Cited by 11 publications

(14 citation statements)

References 51 publications

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“…On the predicted H3 model, we marked the amino acid positions that contained a residue that was not identical to that found in either the H4 or H6 HA sequences. Additionally, we mapped antigenic sites that were previously described for avian influenza viruses bearing H3 [ 30 ]. As expected, we observed that there are more sequence differences among H3 and H6 HA as compared to H3 and H4 ( Fig 2A and 2B ).…”

Section: Resultsmentioning

confidence: 99%

Heterosubtypic immunity increases infectious dose required to infect Mallard ducks with Influenza A virus

et al. 2018

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Previous field and experimental studies have demonstrated that heterosubtypic immunity (HSI) is a potential driver of Influenza A virus (IAV) prevalence and subtype diversity in mallards. Prior infection with IAV can reduce viral shedding during subsequent reinfection with IAV that have genetically related hemagglutinins (HA). In this experiment, we evaluated the effect of HSI conferred by an H3N8 IAV infection against increasing challenge doses of closely (H4N6) and distantly (H6N2) related IAV subtypes in mallards. Two groups of thirty 1-month-old mallards each, were inoculated with 105.9 50% embryo infectious doses (EID50) of an H3N8 virus or a mock-inoculum. One month later, groups of five birds each were challenged with increasing doses of H4N6 or H6N2 virus; age-matched, single infection control ducks were included for all challenges. Results demonstrate that naïve birds were infected after inoculation with 103 and 104 EID50 doses of the H4N6 or H6N2 virus, but not with 102 EID50 doses of either IAV. In contrast, with birds previously infected with H3N8 IAV, only one duck challenged with 104 EID50 of H4N6 IAV was shedding viral RNA at 2 days post-inoculation, and with H6N2 IAV, only birds challenged with the 104 EID50 dose were positive to virus isolation. Viral shedding in ducks infected with H6N2 IAV was reduced on days 2 and 3 post-inoculation compared to control birds. To explain the differences in the dose necessary to produce infection among H3-primed ducks challenged with H4N6 or H6N2 IAV, we mapped the amino acid sequence changes between H3 and H4 or H6 HA on predicted three-dimensional structures. Most of the sequence differences occurred between H3 and H6 at antigenic sites A, B, and D of the HA1 region. These findings demonstrate that the infectious dose necessary to infect mallards with IAV can increase as a result of HSI and that this effect is most pronounced when the HA of the viruses are genetically related.

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Section: Resultsmentioning

confidence: 99%

Heterosubtypic immunity increases infectious dose required to infect Mallard ducks with Influenza A virus

et al. 2018

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“…The prevalence of IAV infection is up to 30% among wild birds (2), and virus transmission typically occurs via exposure to virus shed in the feces of infected animals (3,4). It has been conceptually proposed that antigenic evolution in migratory waterfowl could be static (5); this theory is supported by recent studies indicating a lack of antigenic diversity among H3 and H7 IAVs in migratory waterfowl in North America (6,7).…”

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Feral Swine in the United States Have Been Exposed to both Avian and Swine Influenza A Viruses

Martin

Sun

Carrel

et al. 2017

Appl Environ Microbiol

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Influenza A viruses (IAVs) in swine can cause sporadic infections and pandemic outbreaks among humans, but how avian IAV emerges in swine is still unclear. Unlike domestic swine, feral swine are free ranging and have many opportunities for IAV exposure through contacts with various habitats and animals, including migratory waterfowl, a natural reservoir for IAVs. During the period from 2010 to 2013, 8,239 serum samples were collected from feral swine across 35 U.S. states and tested against 45 contemporary antigenic variants of avian, swine, and human IAVs; of these, 406 (4.9%) samples were IAV antibody positive. Among 294 serum samples selected for antigenic characterization, 271 cross-reacted with ≥1 tested virus, whereas the other 23 did not cross-react with any tested virus. Of the 271 IAV-positive samples, 236 cross-reacted with swine IAVs, 1 with avian IAVs, and 16 with avian and swine IAVs, indicating that feral swine had been exposed to both swine and avian IAVs but predominantly to swine IAVs. Our findings suggest that feral swine could potentially be infected with both avian and swine IAVs, generating novel IAVs by hosting and reassorting IAVs from wild birds and domestic swine and facilitating adaptation of avian IAVs to other hosts, including humans, before their spillover. Continued surveillance to monitor the distribution and antigenic diversities of IAVs in feral swine is necessary to increase our understanding of the natural history of IAVs. There are more than 5 million feral swine distributed across at least 35 states in the United States. In contrast to domestic swine, feral swine are free ranging and have unique opportunities for contact with wildlife, livestock, and their habitats. Our serological results indicate that feral swine in the United States have been exposed to influenza A viruses (IAVs) consistent with those found in both domestic swine and wild birds, with the predominant infections consisting of swine-adapted IAVs. Our findings suggest that feral swine have been infected with IAVs at low levels and could serve as hosts for the generation of novel IAVs at the interface of feral swine, wild birds, domestic swine, and humans.

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“…Furthermore, within other host systems, evasion of IAV-specific antibodies by IAVs-called antigenic variation-has been described for seasonal human IAVs (18,19), swine IAVs (20)(21)(22), and equine IAVs (23) and for highly pathogenic avian influenza viruses (HPAIVs) that circulate in poultry (24,25). Despite numerous studies on the genetic variation of LPAIVs in wild birds, the antigenic variation within LPAIV subtypes that circulate in wild birds has barely been investigated (26,27).…”

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Phylogeography and Antigenic Diversity of Low-Pathogenic Avian Influenza H13 and H16 Viruses

Verhagen

Poen²,

Stallknecht

et al. 2020

J Virol

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Low-pathogenic avian influenza viruses (LPAIVs) are genetically highly variable and have diversified into multiple evolutionary lineages that are primarily associated with wild-bird reservoirs. Antigenic variation has been described for mammalian influenza viruses and for highly pathogenic avian influenza viruses that circulate in poultry, but much less is known about antigenic variation of LPAIVs. In this study, we focused on H13 and H16 LPAIVs that circulate globally in gulls. We investigated the evolutionary history and intercontinental gene flow based on the hemagglutinin (HA) gene and used representative viruses from genetically distinct lineages to determine their antigenic properties by hemagglutination inhibition assays. For H13, at least three distinct genetic clades were evident, while for H16, at least two distinct genetic clades were evident. Twenty and ten events of intercontinental gene flow were identified for H13 and H16 viruses, respectively. At least two antigenic variants of H13 and at least one antigenic variant of H16 were identified. Amino acid positions in the HA protein that may be involved in the antigenic variation were inferred, and some of the positions were located near the receptor binding site of the HA protein, as they are in the HA protein of mammalian influenza A viruses. These findings suggest independent circulation of H13 and H16 subtypes in gull populations, as antigenic patterns do not overlap, and they contribute to the understanding of the genetic and antigenic variation of LPAIVs naturally circulating in wild birds. IMPORTANCE Wild birds play a major role in the epidemiology of low-pathogenic avian influenza viruses (LPAIVs), which are occasionally transmitted—directly or indirectly—from them to other species, including domestic animals, wild mammals, and humans, where they can cause subclinical to fatal disease. Despite a multitude of genetic studies, the antigenic variation of LPAIVs in wild birds is poorly understood. Here, we investigated the evolutionary history, intercontinental gene flow, and antigenic variation among H13 and H16 LPAIVs. The circulation of subtypes H13 and H16 seems to be maintained by a narrower host range, in particular gulls, than the majority of LPAIV subtypes and may therefore serve as a model for evolution and epidemiology of H1 to H12 LPAIVs in wild birds. The findings suggest that H13 and H16 LPAIVs circulate independently of each other and emphasize the need to investigate within-clade antigenic variation of LPAIVs in wild birds.

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Antigenic Characterization of H3 Subtypes of Avian Influenza A Viruses from North America

Cited by 11 publications

References 51 publications

Heterosubtypic immunity increases infectious dose required to infect Mallard ducks with Influenza A virus

Heterosubtypic immunity increases infectious dose required to infect Mallard ducks with Influenza A virus

Feral Swine in the United States Have Been Exposed to both Avian and Swine Influenza A Viruses

Phylogeography and Antigenic Diversity of Low-Pathogenic Avian Influenza H13 and H16 Viruses

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