Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination

Xiaosong He, Tyson H. Holmes, Mrinmoy Sanyal, Randy A. Albrecht, Adolfo Garciá-Sastre, Cornelia L. Dekker, Mark M. Davis, Harry B. Greenberg

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Background. The human B-cell response to natural influenza virus infection has not been extensively investigated at the polyclonal level. Methods. The overall B-cell response of patients acutely infected with the 2009 pandemic influenza A(H1N1)pdm09 virus (A[H1N1]pdm09) was analyzed by determining the reactivity of plasmablast-derived polyclonal antibodies (PPAbs) to influenza proteins. Recipients of inactivated influenza vaccine containing the same A(H1N1)pdm09 strain were studied for comparison. Results. During acute infection, robust plasmablast responses to the infecting virus were detected, characterized by a greater PPAb reactivity to the conserved influenza virus nuclear protein and to heterovariant and heterosubtypic hemagglutinins, in comparison to responses to the inactivated A(H1N1)pdm09 vaccine. In A(H1N1)pdm09 vaccinees, the presence of baseline serum neutralizing antibodies against A(H1N1)pdm09, suggesting previous exposure to natural A(H1N1)pdm09 infection, did not affect the plasmablast response to vaccination, whereas repeated immunization with inactivated A(H1N1)pdm09 vaccine resulted in significantly reduced vaccine-specific and cross-reactive PPAb responses. Conclusions. Natural A(H1N1)pdm09 infection and inactivated A(H1N1)pdm09 vaccination result in very distinct patterns of B-cell activation and priming. These differences are likely to be associated with differences in protective immunity, especially cross-protection against heterovariant and heterosubtypic influenza virus strains.

Original languageEnglish (US)
Pages (from-to)1051-1059
Number of pages9
JournalJournal of Infectious Diseases
Volume211
Issue number7
DOIs
StatePublished - Apr 1 2015
Externally publishedYes

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Virus Diseases
Orthomyxoviridae
Human Influenza
Vaccination
B-Lymphocytes
Vaccines
Infection
Cross Protection
H1N1 Subtype Influenza A Virus
Inactivated Vaccines
Antibodies
Influenza Vaccines
Hemagglutinins
Pandemics
Nuclear Proteins
Neutralizing Antibodies
Antibody Formation
Immunity
Immunization
Viruses

Keywords

  • antibody
  • B-cell response
  • influenza vaccine
  • influenza virus infection
  • plasmablast

ASJC Scopus subject areas

  • Infectious Diseases
  • Immunology and Allergy

Cite this

He, X., Holmes, T. H., Sanyal, M., Albrecht, R. A., Garciá-Sastre, A., Dekker, C. L., ... Greenberg, H. B. (2015). Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination. Journal of Infectious Diseases, 211(7), 1051-1059. https://doi.org/10.1093/infdis/jiu580

Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination. / He, Xiaosong; Holmes, Tyson H.; Sanyal, Mrinmoy; Albrecht, Randy A.; Garciá-Sastre, Adolfo; Dekker, Cornelia L.; Davis, Mark M.; Greenberg, Harry B.

In: Journal of Infectious Diseases, Vol. 211, No. 7, 01.04.2015, p. 1051-1059.

Research output: Contribution to journalArticle

He, X, Holmes, TH, Sanyal, M, Albrecht, RA, Garciá-Sastre, A, Dekker, CL, Davis, MM & Greenberg, HB 2015, 'Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination', Journal of Infectious Diseases, vol. 211, no. 7, pp. 1051-1059. https://doi.org/10.1093/infdis/jiu580
He, Xiaosong ; Holmes, Tyson H. ; Sanyal, Mrinmoy ; Albrecht, Randy A. ; Garciá-Sastre, Adolfo ; Dekker, Cornelia L. ; Davis, Mark M. ; Greenberg, Harry B. / Distinct patterns of B-cell activation and priming by natural influenza virus infection versus inactivated influenza vaccination. In: Journal of Infectious Diseases. 2015 ; Vol. 211, No. 7. pp. 1051-1059.
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abstract = "Background. The human B-cell response to natural influenza virus infection has not been extensively investigated at the polyclonal level. Methods. The overall B-cell response of patients acutely infected with the 2009 pandemic influenza A(H1N1)pdm09 virus (A[H1N1]pdm09) was analyzed by determining the reactivity of plasmablast-derived polyclonal antibodies (PPAbs) to influenza proteins. Recipients of inactivated influenza vaccine containing the same A(H1N1)pdm09 strain were studied for comparison. Results. During acute infection, robust plasmablast responses to the infecting virus were detected, characterized by a greater PPAb reactivity to the conserved influenza virus nuclear protein and to heterovariant and heterosubtypic hemagglutinins, in comparison to responses to the inactivated A(H1N1)pdm09 vaccine. In A(H1N1)pdm09 vaccinees, the presence of baseline serum neutralizing antibodies against A(H1N1)pdm09, suggesting previous exposure to natural A(H1N1)pdm09 infection, did not affect the plasmablast response to vaccination, whereas repeated immunization with inactivated A(H1N1)pdm09 vaccine resulted in significantly reduced vaccine-specific and cross-reactive PPAb responses. Conclusions. Natural A(H1N1)pdm09 infection and inactivated A(H1N1)pdm09 vaccination result in very distinct patterns of B-cell activation and priming. These differences are likely to be associated with differences in protective immunity, especially cross-protection against heterovariant and heterosubtypic influenza virus strains.",
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AU - Holmes, Tyson H.

AU - Sanyal, Mrinmoy

AU - Albrecht, Randy A.

AU - Garciá-Sastre, Adolfo

AU - Dekker, Cornelia L.

AU - Davis, Mark M.

AU - Greenberg, Harry B.

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N2 - Background. The human B-cell response to natural influenza virus infection has not been extensively investigated at the polyclonal level. Methods. The overall B-cell response of patients acutely infected with the 2009 pandemic influenza A(H1N1)pdm09 virus (A[H1N1]pdm09) was analyzed by determining the reactivity of plasmablast-derived polyclonal antibodies (PPAbs) to influenza proteins. Recipients of inactivated influenza vaccine containing the same A(H1N1)pdm09 strain were studied for comparison. Results. During acute infection, robust plasmablast responses to the infecting virus were detected, characterized by a greater PPAb reactivity to the conserved influenza virus nuclear protein and to heterovariant and heterosubtypic hemagglutinins, in comparison to responses to the inactivated A(H1N1)pdm09 vaccine. In A(H1N1)pdm09 vaccinees, the presence of baseline serum neutralizing antibodies against A(H1N1)pdm09, suggesting previous exposure to natural A(H1N1)pdm09 infection, did not affect the plasmablast response to vaccination, whereas repeated immunization with inactivated A(H1N1)pdm09 vaccine resulted in significantly reduced vaccine-specific and cross-reactive PPAb responses. Conclusions. Natural A(H1N1)pdm09 infection and inactivated A(H1N1)pdm09 vaccination result in very distinct patterns of B-cell activation and priming. These differences are likely to be associated with differences in protective immunity, especially cross-protection against heterovariant and heterosubtypic influenza virus strains.

AB - Background. The human B-cell response to natural influenza virus infection has not been extensively investigated at the polyclonal level. Methods. The overall B-cell response of patients acutely infected with the 2009 pandemic influenza A(H1N1)pdm09 virus (A[H1N1]pdm09) was analyzed by determining the reactivity of plasmablast-derived polyclonal antibodies (PPAbs) to influenza proteins. Recipients of inactivated influenza vaccine containing the same A(H1N1)pdm09 strain were studied for comparison. Results. During acute infection, robust plasmablast responses to the infecting virus were detected, characterized by a greater PPAb reactivity to the conserved influenza virus nuclear protein and to heterovariant and heterosubtypic hemagglutinins, in comparison to responses to the inactivated A(H1N1)pdm09 vaccine. In A(H1N1)pdm09 vaccinees, the presence of baseline serum neutralizing antibodies against A(H1N1)pdm09, suggesting previous exposure to natural A(H1N1)pdm09 infection, did not affect the plasmablast response to vaccination, whereas repeated immunization with inactivated A(H1N1)pdm09 vaccine resulted in significantly reduced vaccine-specific and cross-reactive PPAb responses. Conclusions. Natural A(H1N1)pdm09 infection and inactivated A(H1N1)pdm09 vaccination result in very distinct patterns of B-cell activation and priming. These differences are likely to be associated with differences in protective immunity, especially cross-protection against heterovariant and heterosubtypic influenza virus strains.

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