Diet switch pre-vaccination improves immune response and metabolic status in formerly obese mice.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
18 Apr 2024
18 Apr 2024
Historique:
received:
11
04
2022
accepted:
20
03
2024
medline:
19
4
2024
pubmed:
19
4
2024
entrez:
18
4
2024
Statut:
aheadofprint
Résumé
Metabolic disease is epidemiologically linked to severe complications upon influenza virus infection, thus vaccination is a priority in this high-risk population. Yet, vaccine responses are less effective in these same hosts. Here we examined how the timing of diet switching from a high-fat diet to a control diet affected influenza vaccine efficacy in diet-induced obese mice. Our results demonstrate that the systemic meta-inflammation generated by high-fat diet exposure limited T cell maturation to the memory compartment at the time of vaccination, impacting the recall of effector memory T cells upon viral challenge. This was not improved with a diet switch post-vaccination. However, the metabolic dysfunction of T cells was reversed if weight loss occurred 4 weeks before vaccination, restoring a functional recall response. This corresponded with changes in the systemic obesity-related biomarkers leptin and adiponectin, highlighting the systemic and specific effects of diet on influenza vaccine immunogenicity.
Identifiants
pubmed: 38637722
doi: 10.1038/s41564-024-01677-y
pii: 10.1038/s41564-024-01677-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIAID NIH HHS
ID : 75N93019C00052
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93021C00016
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93019C00052
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93021C00016
Pays : United States
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Bluher, M. Obesity: global epidemiology and pathogenesis. Nat. Rev. Endocrinol. 15, 288–298 (2019).
pubmed: 30814686
doi: 10.1038/s41574-019-0176-8
Honce, R. & Schultz-Cherry, S. Impact of obesity on influenza A virus pathogenesis, immune response, and evolution. Front. Immunol. 10, 1071 (2019).
pubmed: 31134099
pmcid: 6523028
doi: 10.3389/fimmu.2019.01071
Zlotnikov, N. et al. Infection with the Lyme disease pathogen suppresses innate immunity in mice with diet-induced obesity. Cell. Microbiol. 19, e12689 (2017).
pubmed: 27794208
doi: 10.1111/cmi.12689
Weger-Lucarelli, J. et al. Host nutritional status affects alphavirus virulence, transmission, and evolution. PLoS Pathog. 15, e1008089 (2019).
pubmed: 31710653
pmcid: 6872174
doi: 10.1371/journal.ppat.1008089
Chuong, C. et al. Nutritional status impacts dengue virus infection in mice. BMC Biol. 18, 106 (2020).
pubmed: 32854687
pmcid: 7453574
doi: 10.1186/s12915-020-00828-x
Van Kerkhove, M. D. et al. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis. PLoS Med. 8, e1001053 (2011).
pubmed: 21750667
pmcid: 3130021
doi: 10.1371/journal.pmed.1001053
Dietz, W. & Santos-Burgoa, C. Obesity and its implications for COVID-19 mortality. Obesity 28, 1005 (2020).
pubmed: 32237206
doi: 10.1002/oby.22818
Pausé, C., Parker, G. & Gray, L. Resisting the problematisation of fatness in COVID-19: in pursuit of health justice. Int. J. Disaster Risk Reduct. 54, 102021 (2021).
pubmed: 34840940
pmcid: 8606246
doi: 10.1016/j.ijdrr.2020.102021
Kim, Y. H. et al. Diet-induced obesity dramatically reduces the efficacy of a 2009 pandemic H1N1 vaccine in a mouse model. J. Infect. Dis. 205, 244–251 (2012).
pubmed: 22147801
doi: 10.1093/infdis/jir731
Karlsson, E. A. et al. Obesity outweighs protection conferred by adjuvanted influenza vaccination. mBio 7, e01144-6 (2016).
pubmed: 27486196
pmcid: 4981723
doi: 10.1128/mBio.01144-16
Neidich, S. D. et al. Increased risk of influenza among vaccinated adults who are obese. Int. J. Obes. 41, 1324–1330 (2017).
doi: 10.1038/ijo.2017.131
Honce, R. et al. Obesity-related microenvironment promotes emergence of virulent influenza virus strains. mBio 11, e03341-19 (2020).
pubmed: 32127459
pmcid: 7064783
doi: 10.1128/mBio.03341-19
Klein, S. L. & Flanagan, K. L. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626–638 (2016).
pubmed: 27546235
doi: 10.1038/nri.2016.90
Varghese, M., Griffin, C. & Singer, K. The role of sex and sex hormones in regulating obesity-induced inflammation. Adv. Exp. Med. Biol. 1043, 65–86 (2017).
pubmed: 29224091
doi: 10.1007/978-3-319-70178-3_5
Namkoong, H. et al. Obesity worsens the outcome of influenza virus infection associated with impaired type I interferon induction in mice. Biochem. Biophys. Res. Commun. 513, 405–411 (2019).
pubmed: 30967261
doi: 10.1016/j.bbrc.2019.03.211
Baaten, B. J., Li, C.-R. & Bradley, L. M. Multifaceted regulation of T cells by CD44. Commun. Integr. Biol. 3, 508–512 (2010).
pubmed: 21331226
pmcid: 3038050
doi: 10.4161/cib.3.6.13495
Kiran, S., Kumar, V., Murphy, E. A., Enos, R. T. & Singh, U. P. High fat diet-induced CD8+ T cells in adipose tissue mediate macrophages to sustain low-grade chronic inflammation. Front. Immunol. 12, 680944 (2021).
pubmed: 34248964
pmcid: 8261297
doi: 10.3389/fimmu.2021.680944
Myers, M. A. et al. Dynamically linking influenza virus infection kinetics, lung injury, inflammation, and disease severity. eLife 10, e68864 (2021).
pubmed: 34282728
pmcid: 8370774
doi: 10.7554/eLife.68864
Rebeles, J. et al. Obesity-induced changes in T-cell metabolism are associated with impaired memory T-cell response to influenza and are not reversed with weight loss. J. Infect. Dis. 219, 1652–1661 (2019).
pubmed: 30535161
doi: 10.1093/infdis/jiy700
Srikanthan, K., Feyh, A., Visweshwar, H., Shapiro, J. I. & Sodhi, K. Systematic review of metabolic syndrome biomarkers: a panel for early detection, management, and risk stratification in the West Virginian population. Int. J. Med. Sci. 13, 25–38 (2016).
pubmed: 26816492
pmcid: 4716817
doi: 10.7150/ijms.13800
Frühbeck, G., Catalán, V., Rodríguez, A. & Gómez-Ambrosi, J. Adiponectin–leptin ratio: a promising index to estimate adipose tissue dysfunction. Relation with obesity-associated cardiometabolic risk. Adipocyte 7, 57–62 (2018).
pubmed: 29205099
doi: 10.1080/21623945.2017.1402151
Pérez-Pérez, A., Sánchez-Jiménez, F., Vilariño-García, T. & Sánchez-Margalet, V. Role of leptin in inflammation and vice versa. Int. J. Mol. Sci. 21, 5887 (2020).
pubmed: 32824322
pmcid: 7460646
doi: 10.3390/ijms21165887
van Niekerk, G., Christowitz, C., Conradie, D. & Engelbrecht, A.-M. Insulin as an immunomodulatory hormone. Cytokine Growth Factor Rev. 52, 34–44 (2020).
pubmed: 31831339
doi: 10.1016/j.cytogfr.2019.11.006
Zhang, A. J. et al. Leptin mediates the pathogenesis of severe 2009 pandemic influenza A(H1N1) infection associated with cytokine dysregulation in mice with diet-induced obesity. J. Infect. Dis. 207, 1270–1280 (2013).
pubmed: 23325916
doi: 10.1093/infdis/jit031
Cho, W. J. et al. Diet-induced obesity reduces the production of influenza vaccine-induced antibodies via impaired macrophage function. Acta Virol. 60, 298–306 (2016).
pubmed: 27640440
doi: 10.4149/av_2016_03_298
Sheridan, P. A. et al. Obesity is associated with impaired immune response to influenza vaccination in humans. Int. J. Obes. 36, 1072–1077 (2012).
doi: 10.1038/ijo.2011.208
Paich, H. A. et al. Overweight and obese adult humans have a defective cellular immune response to pandemic H1N1 influenza A virus. Obesity 21, 2377–2386 (2013).
pubmed: 23512822
doi: 10.1002/oby.20383
Kalil, A. C. & Thomas, P. G. Influenza virus-related critical illness: pathophysiology and epidemiology. Crit. Care 23, 258 (2019).
pubmed: 31324202
pmcid: 6642581
doi: 10.1186/s13054-019-2539-x
O’Brien, A. et al. Obesity reduces mTORC1 activity in mucosal-associated invariant T cells, driving defective metabolic and functional responses. J. Immunol. 202, 3404–3411 (2019).
pubmed: 31076528
doi: 10.4049/jimmunol.1801600
Andersen, C. J., Murphy, K. E. & Fernandez, M. L. Impact of obesity and metabolic syndrome on immunity. Adv. Nutr. 7, 66–75 (2016).
pubmed: 26773015
pmcid: 4717890
doi: 10.3945/an.115.010207
Frasca, D. & Blomberg, B. B. The impact of obesity and metabolic syndrome on vaccination success. Interdiscip. Top. Gerontol. Geriatr. 43, 86–97 (2020).
pubmed: 32305981
doi: 10.1159/000504440
Corrado, M. & Pearce, E. L. Targeting memory T cell metabolism to improve immunity. J. Clin. Invest. 132, e148546 (2022).
pubmed: 34981777
pmcid: 8718135
doi: 10.1172/JCI148546
Xu, H. C. et al. Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity. Immunity 40, 949–960 (2014).
pubmed: 24909887
doi: 10.1016/j.immuni.2014.05.004
Le, C. T. et al. PD-1 blockade reverses obesity-mediated T cell priming impairment. Front. Immunol. 11, 590568 (2020).
pubmed: 33193426
pmcid: 7658608
doi: 10.3389/fimmu.2020.590568
Herati, R. S. et al. PD-1 directed immunotherapy alters Tfh and humoral immune responses to seasonal influenza vaccine. Nat. Immunol. 23, 1183–1192 (2022).
pubmed: 35902637
pmcid: 9880663
doi: 10.1038/s41590-022-01274-3
Jin, J. et al. Activation of mTORC1 at late endosomes misdirects T cell fate decision in older individuals. Sci. Immunol. 6, eabg0791 (2021).
pubmed: 34145066
pmcid: 8422387
doi: 10.1126/sciimmunol.abg0791
Kiernan, K., Nichols, A. G., Alwarawrah, Y. & MacIver, N. J. Effects of T cell leptin signaling on systemic glucose tolerance and T cell responses in obesity. PLoS ONE 18, e0286470 (2023).
pubmed: 37276236
pmcid: 10241364
doi: 10.1371/journal.pone.0286470
Zani, F. et al. The dietary sweetener sucralose is a negative modulator of T cell-mediated responses. Nature 615, 705–711 (2023).
pubmed: 36922598
pmcid: 10033444
doi: 10.1038/s41586-023-05801-6
Mauro, C. et al. Obesity-induced metabolic stress leads to biased effector memory CD4+ T cell differentiation via PI3K p110δ-Akt-mediated signals. Cell Metab. 25, 593–609 (2017).
pubmed: 28190771
pmcid: 5355363
doi: 10.1016/j.cmet.2017.01.008
Messaoudi, I. et al. Long-lasting effect of obesity on skeletal muscle transcriptome. BMC Genomics 18, 411 (2017).
pubmed: 28545403
pmcid: 5445270
doi: 10.1186/s12864-017-3799-y
Rossi, E. L. et al. Obesity-associated alterations in inflammation, epigenetics, and mammary tumor growth persist in formerly obese mice. Cancer Prev. Res. 9, 339–348 (2016).
doi: 10.1158/1940-6207.CAPR-15-0348
Frasca, D., Diaz, A., Romero, M. & Blomberg, B. B. Leptin induces immunosenescence in human B cells. Cell. Immunol. 348, 103994 (2020).
pubmed: 31831137
doi: 10.1016/j.cellimm.2019.103994
Green, W. D. et al. Inflammation and metabolism of influenza-stimulated peripheral blood mononuclear cells from adults with obesity following bariatric surgery. J. Infect. Dis. 227, 92–102 (2022).
pubmed: 35975968
pmcid: 10205606
doi: 10.1093/infdis/jiac345
Sipe, L. M. et al. Response to immune checkpoint blockade improved in pre-clinical model of breast cancer after bariatric surgery. eLife 11, e79143 (2022).
pubmed: 35775614
pmcid: 9342954
doi: 10.7554/eLife.79143
Pingili, A. K. et al. Immune checkpoint blockade reprograms systemic immune landscape and tumor microenvironment in obesity-associated breast cancer. Cell Rep. 35, 109285 (2021).
pubmed: 34161764
pmcid: 8574993
doi: 10.1016/j.celrep.2021.109285
Pearce, E. L. et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460, 103–107 (2009).
pubmed: 19494812
pmcid: 2803086
doi: 10.1038/nature08097
van der Windt, G. J. W. et al. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 36, 68–78 (2012).
pubmed: 22206904
doi: 10.1016/j.immuni.2011.12.007
Hany, M. et al. Impact of bariatric surgery on the effectiveness of serological response after COVID-19 vaccination. Langenbecks Arch. Surg. 407, 2337–2346 (2022).
pubmed: 35486149
pmcid: 9050480
doi: 10.1007/s00423-022-02516-6
Tylka, T. L. et al. The weight-inclusive versus weight-normative approach to health: evaluating the evidence for prioritizing well-being over weight loss. J. Obes. 2014, 983495 (2014).
pubmed: 25147734
pmcid: 4132299
doi: 10.1155/2014/983495
Aminian, A. et al. Association of weight loss achieved through metabolic surgery with risk and severity of COVID-19 infection. JAMA Surg. https://doi.org/10.1001/jamasurg.2021.6496 (2021).
doi: 10.1001/jamasurg.2021.6496
pmcid: 8717211
Williams, L. M. et al. The development of diet-induced obesity and glucose intolerance in C57BL/6 mice on a high-fat diet consists of distinct phases. PLoS ONE 9, e106159 (2014).
pubmed: 25170916
pmcid: 4149520
doi: 10.1371/journal.pone.0106159
Skinner, R. C., Warren, D. C., Lateef, S. N., Benedito, V. A. & Tou, J. C. Apple pomace consumption favorably alters hepatic lipid metabolism in young female Sprague-Dawley rats fed a western diet. Nutrients 10, E1882 (2018).
doi: 10.3390/nu10121882
Reber, A. & Katz, J. Immunological assessment of influenza vaccines and immune correlates of protection. Expert Rev. Vaccines 12, 519–536 (2013).
pubmed: 23659300
pmcid: 9002926
doi: 10.1586/erv.13.35
Rowe, T. et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J. Clin. Microbiol. 37, 937–943 (1999).
pubmed: 10074505
pmcid: 88628
doi: 10.1128/JCM.37.4.937-943.1999
Anderson, K. G. et al. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9, 209–222 (2014).
pubmed: 24385150
pmcid: 4428344
doi: 10.1038/nprot.2014.005
de Brito Monteiro, L., Davanzo, G. G., de Aguiar, C. F. & Moraes-Vieira, P. M. M. Using flow cytometry for mitochondrial assays. MethodsX 7, 100938 (2020).
doi: 10.1016/j.mex.2020.100938
Pengcheng, L., Lu, J. L. & Koestler, D. pwr2: Power and Sample Size Analysis for One-Way and Two-Way ANOVA Models https://cran.r-project.org/web/packages/pwr2/pwr2.pdf (2017).
Ben-Shachar, M., Lüdecke, D. & Makowski, D. Effectsize: estimation of effect size indices and standardized parameters. J. Open Source Softw. 5, 2815 (2020).
doi: 10.21105/joss.02815
Meliopoulos, V. A. et al. An epithelial integrin regulates the amplitude of protective lung interferon responses against multiple respiratory pathogens. PLoS Pathog. 12, e1005804 (2016).
pubmed: 27505057
pmcid: 4978498
doi: 10.1371/journal.ppat.1005804