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Seasonal Variability and Shared Molecular Signatures of Inactivated Influenza Vaccination in Young and Older Adults

Stefan Avey, Subhasis Mohanty, Daniel G. Chawla, Hailong Meng, Thilinie Bandaranayake, Ikuyo Ueda, Heidi J. Zapata, Koonam Park, Tamara P. Blevins, Sui Tsang, Robert B. Belshe, Susan M. Kaech, Albert C. Shaw and Steven H. Kleinstein
J Immunol February 14, 2020, ji1900922; DOI: https://doi.org/10.4049/jimmunol.1900922
Stefan Avey
*Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511;
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Subhasis Mohanty
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Daniel G. Chawla
*Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511;
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Hailong Meng
‡Department of Pathology, Yale School of Medicine, New Haven, CT 06520;
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Thilinie Bandaranayake
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Ikuyo Ueda
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Heidi J. Zapata
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Koonam Park
§Department of Immunobiology, Yale School of Medicine, New Haven, CT 06520; and
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Tamara P. Blevins
¶Division of Infectious Diseases, Department of Medicine, Saint Louis University School of Medicine, St. Louis, MO 63104
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Sui Tsang
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Robert B. Belshe
¶Division of Infectious Diseases, Department of Medicine, Saint Louis University School of Medicine, St. Louis, MO 63104
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Susan M. Kaech
§Department of Immunobiology, Yale School of Medicine, New Haven, CT 06520; and
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Albert C. Shaw
†Section of Infectious Diseases, Department of Internal Medicine, Yale School of Medicine, New Haven, CT 06520;
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Steven H. Kleinstein
*Interdepartmental Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511;
‡Department of Pathology, Yale School of Medicine, New Haven, CT 06520;
§Department of Immunobiology, Yale School of Medicine, New Haven, CT 06520; and
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Key Points

  • Consistent transcriptional signatures were identified 28 d after influenza vaccination.

  • A new end point (maxRBA) characterizes Ab response relative to baseline.

  • Genes related to Ab response behave differently in young and older adults.

Abstract

The seasonal influenza vaccine is an important public health tool but is only effective in a subset of individuals. The identification of molecular signatures provides a mechanism to understand the drivers of vaccine-induced immunity. Most previously reported molecular signatures of human influenza vaccination were derived from a single age group or season, ignoring the effects of immunosenescence or vaccine composition. Thus, it remains unclear how immune signatures of vaccine response change with age across multiple seasons. In this study we profile the transcriptional landscape of young and older adults over five consecutive vaccination seasons to identify shared signatures of vaccine response as well as marked seasonal differences. Along with substantial variability in vaccine-induced signatures across seasons, we uncovered a common transcriptional signature 28 days postvaccination in both young and older adults. However, gene expression patterns associated with vaccine-induced Ab responses were distinct in young and older adults; for example, increased expression of killer cell lectin-like receptor B1 (KLRB1; CD161) 28 days postvaccination positively and negatively predicted vaccine-induced Ab responses in young and older adults, respectively. These findings contribute new insights for developing more effective influenza vaccines, particularly in older adults.

Footnotes

  • This work was supported by National Institutes of Health (NIH) Grants U19 AI089992 and K24 AG042489 and by the Claude D. Pepper Older Americans Independence Center at Yale (P30 AG021342). Computational resources and support were provided by the Yale Center for Research Computing (NIH Grants RR19895 and RR029676-01). H.J.Z. was supported by a GEMSSTAR award from the National Institute on Aging (R03 AG050947). D.G.C. was supported by NIH Training Grant T32 EB019941. T.B. was supported by NIH/National Institute of Allergy and Infectious Diseases T32 AI07517. S.A. was supported by the National Science Foundation (NSF) Graduate Research Fellowship Program (Grant DGE-1122492). Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF.

  • The microarray data presented in this article have been submitted to the Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/) under accession numbers GSE65440, GSE65442, GSE95584, GSE101709, and GSE101710.

  • The online version of this article contains supplemental material.

  • Received August 7, 2019.
  • Accepted January 8, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Seasonal Variability and Shared Molecular Signatures of Inactivated Influenza Vaccination in Young and Older Adults
Stefan Avey, Subhasis Mohanty, Daniel G. Chawla, Hailong Meng, Thilinie Bandaranayake, Ikuyo Ueda, Heidi J. Zapata, Koonam Park, Tamara P. Blevins, Sui Tsang, Robert B. Belshe, Susan M. Kaech, Albert C. Shaw, Steven H. Kleinstein
The Journal of Immunology February 14, 2020, ji1900922; DOI: 10.4049/jimmunol.1900922

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Seasonal Variability and Shared Molecular Signatures of Inactivated Influenza Vaccination in Young and Older Adults
Stefan Avey, Subhasis Mohanty, Daniel G. Chawla, Hailong Meng, Thilinie Bandaranayake, Ikuyo Ueda, Heidi J. Zapata, Koonam Park, Tamara P. Blevins, Sui Tsang, Robert B. Belshe, Susan M. Kaech, Albert C. Shaw, Steven H. Kleinstein
The Journal of Immunology February 14, 2020, ji1900922; DOI: 10.4049/jimmunol.1900922
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Print ISSN 0022-1767        Online ISSN 1550-6606