The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority
The high genetic and antigenic variability of influenza virus and the repeated exposures of individuals to the virus over time account for the human immune responses toward this pathogen to continuously evolve during the lifespan of an individual. Influenza-specific immune memory to past strains has...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.987984/full |
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| author | Federica Sicca Eleni Sakorafa Anouk de Jonge Jacqueline de Vries-Idema Fan Zhou Fan Zhou Rebecca Jane Cox Rebecca Jane Cox Anke Huckriede |
| author_facet | Federica Sicca Eleni Sakorafa Anouk de Jonge Jacqueline de Vries-Idema Fan Zhou Fan Zhou Rebecca Jane Cox Rebecca Jane Cox Anke Huckriede |
| author_sort | Federica Sicca |
| collection | DOAJ |
| description | The high genetic and antigenic variability of influenza virus and the repeated exposures of individuals to the virus over time account for the human immune responses toward this pathogen to continuously evolve during the lifespan of an individual. Influenza-specific immune memory to past strains has been shown to affect the immune responses to subsequent influenza strains and in turn to be changed itself through the new virus encounter. However, exactly how and to what extent this happens remains unclear. Here we studied pre-existing immunity against influenza A virus (IAV) by assessing IAV binding (IgG), neutralizing, and neuraminidase-specific antibodies to 5 different IAV strains in 180 subjects from 3 different age cohorts, adolescents, adults, and elderly, over a 5-year time span. In each age cohort, the highest neutralizing antibody titers were seen for a virus strain that circulated early in their life but the highest increase in titer was found for the most recent virus strains. In contrast, the highest IgG titers were seen against recent virus strains but the biggest increase in titer occurred against older strains. Significant increases in neutralizing antibody titers against a newly encountered virus strain were observed in all age cohorts demonstrating that pre-existing immunity did not hamper antibody induction. Our results indicate that the evolution of influenza-specific humoral immunity differs for rather cross-reactive virus-binding antibodies and more strain-specific neutralizing antibodies. Nevertheless, in general, our observations lend support to the antigenic seniority theory according to which the antibody response to influenza is broadened with each virus encounter, with the earliest encountered strain taking in the most senior and thus dominant position. |
| first_indexed | 2024-04-11T13:19:49Z |
| format | Article |
| id | doaj.art-fd4b7d186c1e4d6ea00b5afca79a4f3f |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T13:19:49Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-fd4b7d186c1e4d6ea00b5afca79a4f3f2022-12-22T04:22:15ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-09-011310.3389/fimmu.2022.987984987984The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniorityFederica Sicca0Eleni Sakorafa1Anouk de Jonge2Jacqueline de Vries-Idema3Fan Zhou4Fan Zhou5Rebecca Jane Cox6Rebecca Jane Cox7Anke Huckriede8Department of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, NetherlandsDepartment of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, NetherlandsDepartment of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, NetherlandsDepartment of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, NetherlandsInfluenza Centre, Department of Clinical Science, University of Bergen, Bergen, NorwayDepartment Microbiology, Haukeland University Hospital, Bergen, NorwayInfluenza Centre, Department of Clinical Science, University of Bergen, Bergen, NorwayDepartment Microbiology, Haukeland University Hospital, Bergen, NorwayDepartment of Medical Microbiology, University of Groningen, University Medical Center Groningen, Groningen, NetherlandsThe high genetic and antigenic variability of influenza virus and the repeated exposures of individuals to the virus over time account for the human immune responses toward this pathogen to continuously evolve during the lifespan of an individual. Influenza-specific immune memory to past strains has been shown to affect the immune responses to subsequent influenza strains and in turn to be changed itself through the new virus encounter. However, exactly how and to what extent this happens remains unclear. Here we studied pre-existing immunity against influenza A virus (IAV) by assessing IAV binding (IgG), neutralizing, and neuraminidase-specific antibodies to 5 different IAV strains in 180 subjects from 3 different age cohorts, adolescents, adults, and elderly, over a 5-year time span. In each age cohort, the highest neutralizing antibody titers were seen for a virus strain that circulated early in their life but the highest increase in titer was found for the most recent virus strains. In contrast, the highest IgG titers were seen against recent virus strains but the biggest increase in titer occurred against older strains. Significant increases in neutralizing antibody titers against a newly encountered virus strain were observed in all age cohorts demonstrating that pre-existing immunity did not hamper antibody induction. Our results indicate that the evolution of influenza-specific humoral immunity differs for rather cross-reactive virus-binding antibodies and more strain-specific neutralizing antibodies. Nevertheless, in general, our observations lend support to the antigenic seniority theory according to which the antibody response to influenza is broadened with each virus encounter, with the earliest encountered strain taking in the most senior and thus dominant position.https://www.frontiersin.org/articles/10.3389/fimmu.2022.987984/fullinfluenza virusantibodiesstrain-specificitylongitudinal cohortH1N1pdm09 |
| spellingShingle | Federica Sicca Eleni Sakorafa Anouk de Jonge Jacqueline de Vries-Idema Fan Zhou Fan Zhou Rebecca Jane Cox Rebecca Jane Cox Anke Huckriede The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority Frontiers in Immunology influenza virus antibodies strain-specificity longitudinal cohort H1N1pdm09 |
| title | The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| title_full | The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| title_fullStr | The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| title_full_unstemmed | The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| title_short | The evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| title_sort | evolution of humoral immune responses to past and novel influenza virus strains gives evidence for antigenic seniority |
| topic | influenza virus antibodies strain-specificity longitudinal cohort H1N1pdm09 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.987984/full |
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