Similar humoral responses but distinct CD4
Humans
Influenza Vaccines
/ immunology
Squalene
/ pharmacology
CD4-Positive T-Lymphocytes
/ immunology
Polysorbates
/ pharmacology
Aged
Transcriptome
Adjuvants, Immunologic
Male
Female
Influenza, Human
/ immunology
Immunity, Humoral
/ immunology
Gene Expression Profiling
Influenza A Virus, H3N2 Subtype
/ immunology
Vaccination
Aged, 80 and over
Antibodies, Viral
/ immunology
CD4+ T cells
Gene expression profiling
High-dose influenza vaccine
MF59-adjuvanted influenza vaccine
Older adults
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 Oct 2024
18 Oct 2024
Historique:
received:
11
04
2024
accepted:
03
10
2024
medline:
19
10
2024
pubmed:
19
10
2024
entrez:
18
10
2024
Statut:
epublish
Résumé
Older age (≥ 65 years) is associated with impaired responses to influenza vaccination, leading to the preferential recommendation of MF59-adjuvanted (MF59Flu) or high-dose (HDFlu) influenza vaccines for this age group in the United States. Herein, we characterized transcriptomic profiles of CD4
Identifiants
pubmed: 39424894
doi: 10.1038/s41598-024-75250-2
pii: 10.1038/s41598-024-75250-2
doi:
Substances chimiques
Influenza Vaccines
0
MF59 oil emulsion
0
Squalene
7QWM220FJH
Polysorbates
0
Adjuvants, Immunologic
0
Antibodies, Viral
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
24420Subventions
Organisme : National Institute of Allergy and Infectious Diseases
ID : R01AI132348
Organisme : NIAID NIH HHS
ID : 75N93019C00052
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
Goodwin, K., Viboud, C. & Simonsen, L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine. 24, 1159–1169. https://doi.org/10.1016/j.vaccine.2005.08.105 (2006).
doi: 10.1016/j.vaccine.2005.08.105
pubmed: 16213065
Allen, J. C., Toapanta, F. R., Chen, W. & Tennant, S. M. Understanding immunosenescence and its impact on vaccination of older adults. Vaccine. 38, 8264–8272. https://doi.org/10.1016/j.vaccine.2020.11.002 (2020).
doi: 10.1016/j.vaccine.2020.11.002
pubmed: 33229108
pmcid: 7719605
Goronzy, J. J. & Weyand, C. M. Understanding immunosenescence to improve responses to vaccines. Nat. Immunol. 14, 428–436 (2013).
doi: 10.1038/ni.2588
pubmed: 23598398
pmcid: 4183346
Haq, K. & McElhaney, J. E. Immunosenescence: influenza vaccination and the elderly. Curr. Opin. Immunol. 29, 38–42 (2014).
doi: 10.1016/j.coi.2014.03.008
pubmed: 24769424
Krammer, F. et al. Influenza. Nat. Rev. Dis. Primers. 4, 3. https://doi.org/10.1038/s41572-018-0002-y (2018).
doi: 10.1038/s41572-018-0002-y
pubmed: 29955068
pmcid: 7097467
United Nations Department of Economic and Social Affairs, Population Division. World Population Prospects 2022: Summary of Results. UN DESA/POP/2022/TR/NO. 3. https://www.un.org/development/desa/pd/sites/www.un.org.development.desa.pd/files/wpp2022_summary_of_results.pdf (2022).
Cowling, B. J. et al. Comparative immunogenicity of several enhanced influenza vaccine options for older adults: a Randomized, Controlled Trial. Clin. Infect. Dis. 71, 1704–1714. https://doi.org/10.1093/cid/ciz1034 (2020).
doi: 10.1093/cid/ciz1034
pubmed: 31828291
DiazGranados, C. A. et al. Efficacy of high-dose versus standard-dose influenza vaccine in older adults. N. Engl. J. Med. 371, 635–645 (2014).
doi: 10.1056/NEJMoa1315727
pubmed: 25119609
Domnich, A. et al. Effectiveness of MF59-adjuvanted seasonal influenza vaccine in the elderly: a systematic review and meta-analysis. Vaccine. 35, 513–520. https://doi.org/10.1016/j.vaccine.2016.12.011 (2017).
doi: 10.1016/j.vaccine.2016.12.011
pubmed: 28024956
Frey, S. E. et al. Comparison of the safety and immunogenicity of an MF59
doi: 10.1016/j.vaccine.2014.07.013
pubmed: 25045825
Gravenstein, S. et al. Comparative effectiveness of high-dose versus standard-dose influenza vaccination on numbers of US nursing home residents admitted to hospital: a cluster-randomised trial. Lancet Respiratory Med. 5, 738–746 (2017).
doi: 10.1016/S2213-2600(17)30235-7
Lapi, F. et al. Adjuvanted versus nonadjuvanted influenza vaccines and risk of hospitalizations for pneumonia and cerebro/cardiovascular events in the elderly. Expert Rev. Vaccines. 18, 663–670 (2019).
doi: 10.1080/14760584.2019.1622418
pubmed: 31155968
McConeghy, K. W. et al. Cluster-randomized Trial of Adjuvanted Versus Nonadjuvanted Trivalent Influenza Vaccine in 823 US nursing homes. Clin. Infect. Dis. 73, e4237–e4243 (2021).
doi: 10.1093/cid/ciaa1233
pubmed: 32882710
Domnich, A. & de Waure, C. Comparative effectiveness of adjuvanted versus high-dose seasonal influenza vaccines for older adults: a systematic review and meta-analysis. Int. J. Infect. Dis. 122, 855–863. https://doi.org/10.1016/j.ijid.2022.07.048 (2022).
doi: 10.1016/j.ijid.2022.07.048
pubmed: 35878803
Schmader, K. E. et al. Immunogenicity of adjuvanted versus high-dose inactivated influenza vaccines in older adults: a randomized clinical trial. Immun. Ageing. 20, 30. https://doi.org/10.1186/s12979-023-00355-7 (2023).
doi: 10.1186/s12979-023-00355-7
pubmed: 37393237
pmcid: 10314373
McElhaney, J. E. et al. T cell responses are better correlates of vaccine protection in the elderly. J. Immunol. 176, 6333–6339. https://doi.org/10.4049/jimmunol.176.10.6333 (2006).
doi: 10.4049/jimmunol.176.10.6333
pubmed: 16670345
Rosendahl Huber, S. K. et al. Immunogenicity of influenza vaccines: evidence for differential effect of secondary vaccination on humoral and cellular immunity. Front. Immunol. 9, 3103 (2019).
doi: 10.3389/fimmu.2018.03103
pubmed: 30761157
pmcid: 6362424
Chen, W. H. et al. Antibody and Th1-type cell-mediated immune responses in elderly and young adults immunized with the standard or a high dose influenza vaccine. Vaccine. 29, 2865–2873 (2011).
doi: 10.1016/j.vaccine.2011.02.017
pubmed: 21352939
pmcid: 3070775
Jansen, J. M., Gerlach, T., Elbahesh, H., Rimmelzwaan, G. F. & Saletti, G. Influenza virus-specific CD4 + and CD8 + T cell-mediated immunity induced by infection and vaccination. J. Clin. Virol. 119, 44–52. https://doi.org/10.1016/j.jcv.2019.08.009 (2019).
doi: 10.1016/j.jcv.2019.08.009
pubmed: 31491709
Sant, A. J., DiPiazza, A. T., Nayak, J. L., Rattan, A. & Richards, K. A. CD4 T cells in protection from influenza virus: viral antigen specificity and functional potential. Immunol. Rev. 284, 91–105. https://doi.org/10.1111/imr.12662 (2018).
doi: 10.1111/imr.12662
pubmed: 29944766
pmcid: 6070306
Zens, K. D. & Farber, D. L. Memory CD4 T cells in influenza. Curr. Top. Microbiol. Immunol. 386, 399–421. https://doi.org/10.1007/82_2014_401 (2015).
doi: 10.1007/82_2014_401
pubmed: 25005927
pmcid: 4339101
Haralambieva, I. H. et al. T Cell Transcriptional Signatures of Influenza A/H3N2 antibody response to high dose influenza and Adjuvanted Influenza Vaccine in older adults. Viruses. 14, 2763 (2022).
doi: 10.3390/v14122763
pubmed: 36560767
pmcid: 9786771
Zhou, H. et al. Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993–2008. Clin. Infect. Dis. 54, 1427–1436. https://doi.org/10.1093/cid/cis211 (2012).
doi: 10.1093/cid/cis211
pubmed: 22495079
pmcid: 3334364
Reichert, T. A. et al. Influenza and the winter increase in mortality in the United States, 1959–1999. Am. J. Epidemiol. 160, 492–502. https://doi.org/10.1093/aje/kwh227 (2004).
doi: 10.1093/aje/kwh227
pubmed: 15321847
Belongia, E. A. et al. Variable influenza vaccine effectiveness by subtype: a systematic review and meta-analysis of test-negative design studies. Lancet. Infect. Dis. 16, 942–951 (2016).
doi: 10.1016/S1473-3099(16)00129-8
pubmed: 27061888
Beyer, W., Palache, A., Lüchters, G., Nauta, J. & Osterhaus, A. Seroprotection rate, mean Fold increase, seroconversion rate: which parameter adequately expresses seroresponse to influenza vaccination?. Virus Res. 103, 125–132 (2004).
doi: 10.1016/j.virusres.2004.02.024
pubmed: 15163500
Luckheeram, R. V., Zhou, R., Verma, A. D. & Xia, B. CD4⁺T cells: differentiation and functions. Clin. Dev. Immunol. 2012, 925135. https://doi.org/10.1155/2012/925135 (2012).
Swain, S. L., McKinstry, K. K. & Strutt, T. M. Expanding roles for CD4 + T cells in immunity to viruses. Nat. Rev. Immunol. 12, 136–148. https://doi.org/10.1038/nri3152 (2012).
doi: 10.1038/nri3152
pmcid: 3764486
Prigge, A. D., Ma, R., Coates, B. M., Singer, B. D. & Ridge, K. M. Age-dependent differences in T-Cell responses to Influenza A Virus. Am. J. Respir Cell. Mol. Biol. 63, 415–423. https://doi.org/10.1165/rcmb.2020-0169TR (2020).
doi: 10.1165/rcmb.2020-0169TR
pubmed: 32609537
pmcid: 7528914
Gaur, P., Munjhal, A. & Lal, S. K. Influenza virus and cell signaling pathways. Med. Sci. Monit. 17, Ra148-154. https://doi.org/10.12659/msm.881801 (2011).
Shapira, S. D. et al. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell. 139, 1255–1267. https://doi.org/10.1016/j.cell.2009.12.018 (2009).
doi: 10.1016/j.cell.2009.12.018
pubmed: 20064372
pmcid: 2892837
Ko, E. J. & Kang, S. M. Immunology and efficacy of MF59-adjuvanted vaccines. Hum. Vaccin Immunother. 14, 3041–3045. https://doi.org/10.1080/21645515.2018.1495301 (2018).
doi: 10.1080/21645515.2018.1495301
pubmed: 30015572
pmcid: 6343625
O’Hagan, D. T., Ott, G. S., De Gregorio, E. & Seubert, A. The mechanism of action of MF59 – an innately attractive adjuvant formulation. Vaccine. 30, 4341–4348. https://doi.org/10.1016/j.vaccine.2011.09.061 (2012).
doi: 10.1016/j.vaccine.2011.09.061
pubmed: 22682289
DiazGranados, C. A. et al. Efficacy of high-dose versus standard-dose influenza vaccine in older adults. N. Engl. J. Med. 371, 635–645. https://doi.org/10.1056/NEJMoa1315727 (2014).
doi: 10.1056/NEJMoa1315727
pubmed: 25119609
Chen, G. et al. Identification of critical genes and pathways for Influenza A Virus infections via Bioinformatics Analysis. Viruses. 14. https://doi.org/10.3390/v14081625 (2022).
Zhang, W. & Liu, H. T. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12, 9–18. https://doi.org/10.1038/sj.cr.7290105 (2002).
doi: 10.1038/sj.cr.7290105
pubmed: 11942415
Basu, S., Binder, R. J., Suto, R., Anderson, K. M. & Srivastava, P. K. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int. Immunol. 12, 1539–1546. https://doi.org/10.1093/intimm/12.11.1539 (2000).
doi: 10.1093/intimm/12.11.1539
pubmed: 11058573
Wu, S., Zhao, Y., Wang, D. & Chen, Z. Mode of Action of Heat shock protein (HSP) inhibitors against viruses through host HSP and Virus interactions. Genes. 14, 792 (2023).
doi: 10.3390/genes14040792
pubmed: 37107550
pmcid: 10138296
Zhang, X. & Yu, W. Heat shock proteins and viral infection. Front. Immunol. 13, 947789. https://doi.org/10.3389/fimmu.2022.947789 (2022).
doi: 10.3389/fimmu.2022.947789
pubmed: 35990630
pmcid: 9389079
Haralambieva, I. H. et al. The impact of immunosenescence on humoral immune response variation after influenza A/H1N1 vaccination in older subjects. PloS One. 10, e0122282 (2015).
doi: 10.1371/journal.pone.0122282
pubmed: 25816015
pmcid: 4376784
Quach, H. Q. et al. The influence of sex, BMI, and age on cellular and humoral immune responses against measles after a 3rd dose of MMR vaccine. J. Infect. Dis. https://doi.org/10.1093/infdis/jiac351 (2022).
doi: 10.1093/infdis/jiac351
pubmed: 35994504
pmcid: 10205623
Voigt, E. A. et al. Sex differences in older adults’ immune responses to seasonal influenza vaccination. Front. Immunol. 10, 180 (2019).
doi: 10.3389/fimmu.2019.00180
pubmed: 30873150
pmcid: 6400991
Goldberg, E. L., Shaw, A. C. & Montgomery, R. R. How inflammation blunts innate immunity in aging. Interdiscip Top. Gerontol. Geriatr. 43, 1–17. https://doi.org/10.1159/000504480 (2020).
doi: 10.1159/000504480
pubmed: 32294641
pmcid: 8063508
Wild, K. et al. Pre-existing immunity and vaccine history determine hemagglutinin-specific CD4 T cell and IgG response following seasonal influenza vaccination. Nat. Commun. 12, 6720. https://doi.org/10.1038/s41467-021-27064-3 (2021).
doi: 10.1038/s41467-021-27064-3
pubmed: 34795301
pmcid: 8602312
Gao, F. X. et al. Extended SARS-CoV-2 RBD booster vaccination induces humoral and cellular immune tolerance in mice. iScience. 25, 105479. https://doi.org/10.1016/j.isci.2022.105479 (2022).
doi: 10.1016/j.isci.2022.105479
pubmed: 36338436
pmcid: 9625849
Uversky, V. N., Redwan, E. M., Makis, W. & Rubio-Casillas, A. IgG4 antibodies Induced by repeated vaccination may generate Immune Tolerance to the SARS-CoV-2 Spike Protein. Vaccines (Basel). 11. https://doi.org/10.3390/vaccines11050991 (2023).
Tani, Y. et al. Five doses of the mRNA vaccination potentially suppress ancestral-strain stimulated SARS-CoV2-specific cellular immunity: a cohort study from the Fukushima vaccination community survey, Japan. Front. Immunol. 14, 1240425. https://doi.org/10.3389/fimmu.2023.1240425 (2023).
doi: 10.3389/fimmu.2023.1240425
pubmed: 37662950
pmcid: 10469480
McGargill, M. A. et al. Immune tolerance limits effective immunity to epitopes targeted by universal influenza vaccines. J. Immunol. 204 245.244-245.244. https://doi.org/10.4049/jimmunol.204.Supp.245.4 (2020).
Jacobson, R. M. et al. Profiles of influenza A/H1N1 vaccine response using hemagglutination-inhibition titers. Hum. Vaccin Immunother. 11, 961–969. https://doi.org/10.1080/21645515.2015.1011990 (2015).
doi: 10.1080/21645515.2015.1011990
pubmed: 25835513
pmcid: 4514374
Ohmit, S. E., Petrie, J. G., Cross, R. T., Johnson, E. & Monto, A. S. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccine-induced protection. J. Infect. Dis. 204, 1879–1885. https://doi.org/10.1093/infdis/jir661 (2011).
doi: 10.1093/infdis/jir661
pubmed: 21998477
Petrie, J. G., Ohmit, S. E., Johnson, E., Cross, R. T. & Monto, A. S. Efficacy studies of influenza vaccines: effect of end points used and characteristics of vaccine failures. J. Infect. Dis. 203, 1309–1315. https://doi.org/10.1093/infdis/jir015 (2011).
doi: 10.1093/infdis/jir015
pubmed: 21378375
pmcid: 3069734
Zimmermann, M. T. et al. Integration of Immune Cell populations, mRNA-Seq, and CpG methylation to Better Predict Humoral Immunity to Influenza Vaccination: dependence of mRNA-Seq/CpG methylation on Immune Cell populations. Front. Immunol. 8, 445. https://doi.org/10.3389/fimmu.2017.00445 (2017).
doi: 10.3389/fimmu.2017.00445
pubmed: 28484452
pmcid: 5399034
Haralambieva, I. H. et al. Transcriptional signatures associated with rubella virus-specific humoral immunity after a third dose of MMR vaccine in women of childbearing age. Eur. J. Immunol. 51, 1824–1838. https://doi.org/10.1002/eji.202049054 (2021).
doi: 10.1002/eji.202049054
pubmed: 33818775
pmcid: 9841595
Ovsyannikova, I. G. et al. Gene signatures associated with adaptive humoral immunity following seasonal influenza A/H1N1 vaccination. Genes Immun. 17, 371–379 (2016).
doi: 10.1038/gene.2016.34
pubmed: 27534615
pmcid: 5133148
Haralambieva, I. H. et al. Transcriptional signatures of influenza A/H1N1-specific IgG memory-like B cell response in older individuals. Vaccine. 34, 3993–4002 (2016).
doi: 10.1016/j.vaccine.2016.06.034
pubmed: 27317456
pmcid: 5520794
Kalari, K. R. et al. MAP-RSeq: Mayo analysis pipeline for RNA sequencing. BMC Bioinform. 15, 1–11 (2014).
doi: 10.1186/1471-2105-15-224
Hansen, K. D., Irizarry, R. A. & Wu, Z. Removing technical variability in RNA-seq data using conditional quantile normalization. Biostatistics. 13, 204–216 (2012).
doi: 10.1093/biostatistics/kxr054
pubmed: 22285995
pmcid: 3297825
Hansen, K. D., Irizarry, R. A. & Wu, Z. Removing technical variability in RNA-seq data using conditional quantile normalization. Biostatistics. 13, 204–216. https://doi.org/10.1093/biostatistics/kxr054 (2012).
doi: 10.1093/biostatistics/kxr054
pubmed: 22285995
pmcid: 3297825
Zeger, S. L. & Liang, K. Y. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 42, 121–130 (1986).
Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics. 16, 284–287. https://doi.org/10.1089/omi.2011.0118 (2012).
doi: 10.1089/omi.2011.0118
pubmed: 22455463
pmcid: 3339379
Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 28, 1947–1951. https://doi.org/10.1002/pro.3715 (2019).
doi: 10.1002/pro.3715
pmcid: 6798127
Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M. & Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 51, D587-d592. https://doi.org/10.1093/nar/gkac963 (2023).
doi: 10.1093/nar/gkac963
Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30. https://doi.org/10.1093/nar/28.1.27 (2000).
doi: 10.1093/nar/28.1.27
pmcid: 102409
Storey, J. D. A direct approach to false discovery rates. J. Royal Stat. Soc. Ser. B: Stat. Methodol. 64, 479–498 (2002).
doi: 10.1111/1467-9868.00346
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc.: Ser. B (Methodol.). 57, 289–300 (1995).
doi: 10.1111/j.2517-6161.1995.tb02031.x