Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck

Neus Latorre-Margalef, Justin D. Brown, Alinde Fojtik, Rebecca L. Poulson, Deborah Carter, Monique Franca, David E. Stallknecht

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Our overall hypothesis is that host population immunity directed at multiple antigens will influence the prevalence, diversity and evolution of influenza A virus (IAV) in avian populations where the vast subtype diversity is maintained. To investigate how initial infection influences the outcome of later infections with homologous or heterologous IAV subtypes and how viruses interact through host immune responses, we carried out experimental infections in mallard ducks (Anas platyrhynchos). Mallards were pre-challenged with an H3N8 low-pathogenic IAV and were divided into six groups. At five weeks post H3N8 inoculation, each group was challenged with a different IAV subtype (H4N5, H10N7, H6N2, H12N5) or the same H3N8. Two additional pre-challenged groups were inoculated with the homologous H3N8 virus at weeks 11 and 15 after pre-challenge to evaluate the duration of protection. The results showed that mallards were still resistant to re-infection after 15 weeks. There was a significant reduction in shedding for all pre-challenged groups compared to controls and the outcome of the heterologous challenges varied according to hemagglutinin (HA) phylogenetic relatedness between the viruses used. There was a boost in the H3 antibody titer after re-infection with H4N5, which is consistent with original antigenic sin or antigenic seniority and suggest a putative strategy of virus evasion. These results imply competition between related subtypes that could regulate IAV subtype population dynamics in nature. Collectively, we provide new insights into within-host IAV complex interactions as drivers of IAV antigenic diversity that could allow the circulation of multiple subtypes in wild ducks.

Original languageEnglish (US)
Article numbere1006419
JournalPLoS pathogens
Volume13
Issue number6
DOIs
StatePublished - Jan 1 2017

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Ducks
Influenza A virus
Immunity
Antibodies
Infection
Viruses
H3N8 Subtype Influenza A Virus
Antigenic Variation
Hemagglutinins
Population Dynamics
Population
Antigens

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Latorre-Margalef, N., Brown, J. D., Fojtik, A., Poulson, R. L., Carter, D., Franca, M., & Stallknecht, D. E. (2017). Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck. PLoS pathogens, 13(6), [e1006419]. https://doi.org/10.1371/journal.ppat.1006419
Latorre-Margalef, Neus ; Brown, Justin D. ; Fojtik, Alinde ; Poulson, Rebecca L. ; Carter, Deborah ; Franca, Monique ; Stallknecht, David E. / Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck. In: PLoS pathogens. 2017 ; Vol. 13, No. 6.
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Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck. / Latorre-Margalef, Neus; Brown, Justin D.; Fojtik, Alinde; Poulson, Rebecca L.; Carter, Deborah; Franca, Monique; Stallknecht, David E.

In: PLoS pathogens, Vol. 13, No. 6, e1006419, 01.01.2017.

Research output: Contribution to journalArticle

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T1 - Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck

AU - Latorre-Margalef, Neus

AU - Brown, Justin D.

AU - Fojtik, Alinde

AU - Poulson, Rebecca L.

AU - Carter, Deborah

AU - Franca, Monique

AU - Stallknecht, David E.

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N2 - Our overall hypothesis is that host population immunity directed at multiple antigens will influence the prevalence, diversity and evolution of influenza A virus (IAV) in avian populations where the vast subtype diversity is maintained. To investigate how initial infection influences the outcome of later infections with homologous or heterologous IAV subtypes and how viruses interact through host immune responses, we carried out experimental infections in mallard ducks (Anas platyrhynchos). Mallards were pre-challenged with an H3N8 low-pathogenic IAV and were divided into six groups. At five weeks post H3N8 inoculation, each group was challenged with a different IAV subtype (H4N5, H10N7, H6N2, H12N5) or the same H3N8. Two additional pre-challenged groups were inoculated with the homologous H3N8 virus at weeks 11 and 15 after pre-challenge to evaluate the duration of protection. The results showed that mallards were still resistant to re-infection after 15 weeks. There was a significant reduction in shedding for all pre-challenged groups compared to controls and the outcome of the heterologous challenges varied according to hemagglutinin (HA) phylogenetic relatedness between the viruses used. There was a boost in the H3 antibody titer after re-infection with H4N5, which is consistent with original antigenic sin or antigenic seniority and suggest a putative strategy of virus evasion. These results imply competition between related subtypes that could regulate IAV subtype population dynamics in nature. Collectively, we provide new insights into within-host IAV complex interactions as drivers of IAV antigenic diversity that could allow the circulation of multiple subtypes in wild ducks.

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