Systems analysis of immunity to influenza vaccination across multiple years and in diverse populations reveals shared molecular signatures
Open accessAbstract
Systems approaches have been used to describe molecular signatures driving immunity to influenza vaccination in humans. Whether such signatures are similar across multiple seasons and in diverse populations is unknown. We applied systems approaches to study immune responses in young, elderly, and diabetic subjects vaccinated with the seasonal influenza vaccine across five consecutive seasons. Signatures of innate immunity and plasmablasts correlated with and predicted influenza antibody titers at 1 month after vaccination with >80% accuracy across multiple seasons but were not associated with the longevity of the response. Baseline signatures of lymphocyte and monocyte inflammation were positively and negatively correlated, respectively, with antibody responses at 1 month. Finally, integrative analysis of microRNAs and transcriptomic profiling revealed potential regulators of vaccine immunity. These results identify shared vaccine-induced signatures across multiple seasons and in diverse populations and might help guide the development of next-generation vaccines that provide persistent immunity against influenza.
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The vaccination-induced innate immune signature is impaired in older individuals.
“This vaccination-induced innate immune signature was impaired in older individuals”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Nakaya et al., 2015
Such inflammatory signatures were more common in older individuals.
“Notably, such signatures were more common in older individuals.”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Nakaya et al., 2015
Early innate responses on the day after influenza vaccination, largely antiviral and type I IFN-related genes, correlate with superior vaccine responses.
“early innate responses on the day after influenza vaccination, largely comprised of antiviral and type I IFN-related genes, correlated with superior vaccine responses.”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Nakaya et al., 2015
In longitudinal annual influenza vaccination studies, inflammatory monocyte transcriptional signatures at baseline consistently correlated with poorer antibody responses, suggesting inflammation is detrimental to protective humoral immunity.
“In longitudinal studies of annual influenza vaccinations, inflammatory monocyte transcriptional signatures at baseline consistently correlated with poorer antibody responses, suggesting that an inflammatory state is detrimental to the establishment of protective humoral immunity”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Nakaya et al., 2015
Pre-vaccination expression of genes associated with T-cell and B-cell function is positively correlated with influenza-specific antibody responses, while monocyte- and inflammation-related genes are negatively correlated.
“Pre-vaccination expression of genes associated with T-cell and B-cell function were positively correlated with influenza-specific antibody responses, while monocyte- and inflammation-related genes were negatively correlated with influenza-specific antibody responses, supporting the concept that inflammatory responses at baseline might be detrimental to vaccine-induced antibody responses [155].”
From Aging of the immune system: Focus on inflammation and vaccination (2016) · cites this paper as [155]
In monocytes, the pre-vaccination expression of genes related to inflammation and innate immune response is negatively correlated to vaccination-induced activation of influenza-specific antibody responses.
“Accordingly, in monocytes, the pre-vaccination expression of genes related to inflammation and innate immune response is negatively correlated to vaccination-induced activation of influenza-specific antibody responses (70).”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [70]
Compared with young and elderly vaccinees from 2010-2011, young subjects showed decreased expression of these modules on day 1 like controls, while antibiotic-treated subjects behaved similarly to elderly vaccinees, who exhibited upregulation post-vaccination.
“we observed that while young subjects showed decreased expression of these modules on day 1 as in the control subjects, antibiotics-treated subjects behaved similarly to elderly vaccinees, who exhibited upregulation of these pathways postvaccination.”
From Antibiotics-Driven Gut Microbiome Perturbation Alters Immunity to Vaccines in Humans (2019) · cites this paper as Nakaya et al., 2015
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- Authors
- Nakaya, H. I., Hagan, T., Duraisingham, S. S., Lee, E. K., Kwissa, M., Rouphael, N., Frasca, D., Gersten, M., Mehta, A. K., Gaujoux, R., Li, G.-M., Gupta, S., Ahmed, R., Mulligan, M. J., Shen-Orr, S., Blomberg, B. B., Subramaniam, S., & Pulendran, B.
- Affiliations
- Emory University (US)
- University of California San Diego (US)
- Churchill Hospital (GB)
- Georgia Institute of Technology (US)
- University of Chicago (US)
- University of Miami (US)
- Technion – Israel Institute of Technology (IL)
- Corresponding author
- Subramaniam, Shankar
- Pulendran, Bali
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2015-12
- Volume
- 43
- Issue
- 6
- Pages
- 1186-1198
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC4859820
- OpenAlex
- W2215687226
- Cited by
- 337
- References
- 55
- Citations by year
- 2026: 16 · 2025: 30 · 2024: 26 · 2023: 30 · 2022: 46 · 2021: 35 · 2020: 38 · 2019: 41 · 2018: 27 · 2017: 34 · 2016: 12 · 2015: 2
- FWCI
- 19.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R37AG023717)
- National Institute of Allergy and Infectious Diseases (R38AI140299, R37 AI48638, U19AI090023, U54AI057157, HHSN272201400004C, P30AI050409, U19AI057266, R37AI048638)
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK057665)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- influenza vaccination, vaccine-induced immunity, seasonal influenza vaccine, antibody response, molecular signatures, innate immunity, plasmablasts, monocyte inflammation, microRNA, gene expression profiling, older adults, diabetes mellitus, cross-population comparison
- MeSH terms
- Adult, Aged, Antibodies, Viral, Female, Flow Cytometry, Humans, Influenza, Human, Influenza Vaccines, Male, Middle Aged, Seasons, Systems Analysis, Oligonucleotide Array Sequence Analysis, Transcriptome
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