Plasmacytoid dendritic cell and myeloid dendritic cell function in ageing: A comparison between elderly and young adult women
Autoři:
Marloes van Splunter aff001; Olaf Perdijk aff001; Henriëtte Fick-Brinkhof aff002; Esther G. Floris-Vollenbroek aff003; Ben Meijer aff001; Sylvia Brugman aff001; Huub F. J. Savelkoul aff001; Els van Hoffen aff003; R. J. Joost van Neerven aff001
Působiště autorů:
Cell Biology and Immunology, Wageningen University, Wageningen, The Netherlands
aff001; Human Nutrition, Wageningen University, Wageningen, The Netherlands
aff002; NIZO Food research, Ede, The Netherlands
aff003; FrieslandCampina, Amersfoort, The Netherlands
aff004
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225825
Souhrn
Ageing is associated with a changing immune system, leading to inflammageing (increased levels of inflammation markers in serum) and immunosenescence (reduced immune cells and reduced responses towards pathogens). This results in reduced vaccination responses and increased infections in elderly. Much is known about the adaptive immune system upon ageing, but less is known about the innate immune system. Therefore, the aim of this study was to compare innate immune function of Toll like receptor (TLR)-mediated responses between elderly and young adult women.
To this end, elderly and young adult women were compared to study the effect of ageing on the relative prevalence and reactivity to TLR-mediated responses of myeloid- and plasmacytoid dendritic cells (mDC, pDC). In addition, TLR expression and inflammatory markers in serum were investigated. Elderly women had reduced numbers of circulating pDCs. In addition, pDCs and mDCs of elderly women responded differently towards TLR stimulation, especially TLR7/8 mediated stimulation was reduced, compared to young adults. In serum, markers involved in inflammation were generally increased in elderly. In conclusion, this study confirms and extends the knowledge about immunosenescence and inflammageing on innate immunity in elderly women.
Klíčová slova:
Cytokines – Immune response – Geriatrics – Aging – Elderly – Young adults – Influenza – Dendritic cells
Zdroje
1. WHO. World report on ageing and health. 2015. doi: 10.1007/s13398-014-0173-7.2
2. Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, et al. A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr. 2013;109: S1–S34.
3. Lesourd B, Mazari L. Nutrition and immunity in elderly. Proc Nutr Soc. 1999;58: 685–695. doi: 10.1017/s0029665199000907 10604204
4. Ventura MT, Casciaro M, Gangemi S, Buquicchio R. Immunosenescence in aging: between immune cells depletion and cytokines up-regulation. Clin Mol Allergy. 2017;15: 21. doi: 10.1186/s12948-017-0077-0 29259496
5. Gameiro CM, Romão F, Castelo-Branco C. Menopause and aging: Changes in the immune system—A review. Maturitas. 2010;67: 316–320. doi: 10.1016/j.maturitas.2010.08.003 20813470
6. Metcalf TU, Cubas RA, Ghneim K, Cartwright MJ, Grevenynghe J Van, Richner JM, et al. Global analyses revealed age-related alterations in innate immune responses after stimulation of pathogen recognition receptors. Aging Cell. 2015;14: 421–432. doi: 10.1111/acel.12320 25728020
7. Shaw AC, Goldstein DR, Montgomery RR. Age-dependent dysregulation of innate immunity. Nat Rev Immunol. 2013;13: 875–887. doi: 10.1038/nri3547 24157572
8. Singh T, Newman AB. Inflammatory markers in population studies of aging. Ageing Res Rev. 2011;10: 319–329. doi: 10.1016/j.arr.2010.11.002 21145432
9. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: A systematic review and meta-analysis. Lancet Infect Dis. 2012;12: 36–44. doi: 10.1016/S1473-3099(11)70295-X 22032844
10. Canaday DH, Amponsay NA, Jones L, Tisch DJ, Hornick TR, Ramachandra L. Influenza-induced production of interferon-alpha is defective in geriatric individuals. J clinidal Immunol. 2010;30: 373–383. doi: 10.1007/s10875-010-9374-9 20182777
11. Friesema IHM, Koppeschaar CE, Donker GA, Dijkstra F, van Noort SP, Smallenburg R, et al. Internet-based monitoring of influenza-like illness in the general population: Experience of five influenza seasons in the Netherlands. Vaccine. 2009;27: 6353–6357. doi: 10.1016/j.vaccine.2009.05.042 19840672
12. Schanzer D, Vachon J, Pelletier L. Age-specific differences in influenza a epidemic curves: Do children drive the spread of influenza epidemics? Am J Epidemiol. 2011;174: 109–117. doi: 10.1093/aje/kwr037 21602300
13. Reichert TA, Simonsen L, Sharma A, Pardo SA, Fedson DS, Miller MA. Influenza and the winter increase in mortality in the United States, 1959–1999. Am J Epidemiol. 2004;160: 492–502. doi: 10.1093/aje/kwh227 15321847
14. Simon AK, Hollander GA, McMichael A. Evolution of the immune system in humans from infancy to old age. Proc R Soc B Biol Sci. 2015;282: 20143085. doi: 10.1098/rspb.2014.3085 26702035
15. Fitzgerald-Bocarsly P, Feng D. The role of type I interferon production by dendritic cells in host defense. Biochimie. 2007;89: 843–855. doi: 10.1016/j.biochi.2007.04.018 17544561
16. Panda A, Qian F, Mohanty S, van Duin D, Newman FK, Zhang L, et al. Age-Associated Decrease in TLR Function in Primary Human Dendritic Cells Predicts Influenza Vaccine Response. J Immunol. 2010;184: 2518–2527. doi: 10.4049/jimmunol.0901022 20100933
17. Jing Y, Shaheen E, Drake RR, Chen N, Gravenstein S, Deng Y. Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Hum Immunol. 2009;70: 777–784. doi: 10.1016/j.humimm.2009.07.005 19596035
18. Franceschi C, Bonafè M, Valensin S, Benedictis GDE. Inflamma-aging An Evolutionary Perspective on Immunosenescence. Ann N Y Acad Sci. 2000;908: 244–254. doi: 10.1111/j.1749-6632.2000.tb06651.x 10911963
19. Franceschi C. Inflammaging as a Major Characteristic of Old People: Can It Be Prevented or Cured? Nutr Rev. 2007;65. doi: 10.1111/j.1753-4887.2007.tb00358.x 18240544
20. Lages CS, Suffia I, Velilla PA, Huang B, Warshaw G, Hildeman DA, et al. Functional Regulatory T Cells Accumulate in Aged Hosts and Promote Chronic Infectious Disease Reactivation. J Immunol. 2008;181: 1835–1848. doi: 10.4049/jimmunol.181.3.1835 18641321
21. Pera A, Campos C, López N, Hassouneh F, Alonso C, Tarazona R, et al. Immunosenescence: Implications for response to infection and vaccination in older people. Maturitas. 2015;82: 50–55. doi: 10.1016/j.maturitas.2015.05.004 26044074
22. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat Rev Immunol. 2008;8: 737–744. doi: 10.1038/nri2394 18728636
23. Meier A, Chang JJ, Chan ES, Pollard RB, Sidhu HK, Kulkarni S, et al. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat Med. 2009;15: 955–959. doi: 10.1038/nm.2004 19597505
24. Seillet C, Laffont S, Trémollières F, Rouquié N, Ribot C, Arnal JF, et al. The TLR-mediated response of plasmacytoid dendritic cells is positively regulated by estradiol in vivo through cell-intrinsic estrogen receptor α signaling. Blood. 2012;119: 454–464. doi: 10.1182/blood-2011-08-371831 22096248
25. van Splunter M, Perdijk O, Fick-Brinkhof H, Feitsma AL, Floris-Vollenbroek EG, Meijer B, et al. Bovine Lactoferrin Enhances TLR7-Mediated Responses in Plasmacytoid Dendritic Cells in Elderly Women: Results From a Nutritional Intervention Study With Bovine Lactoferrin, GOS and Vitamin D. Front Immunol. 2018;9: 1–12. doi: 10.3389/fimmu.2018.00001
26. Garbe K, Bratke K, Wagner S, Virchow JC, Lommatzsch M. Plasmacytoid dendritic cells and their Toll-like receptor 9 expression selectively decrease with age. Hum Immunol. 2012;73: 493–497. doi: 10.1016/j.humimm.2012.02.007 22386694
27. Orsini G, Legitimo A, Failli A, Massei F, Biver P, Consolini R. Enumeration of human peripheral blood dendritic cells throughout the life. Int Immunol. 2012;24: 347–356. doi: 10.1093/intimm/dxs006 22345276
28. Shodell M, Siegal FP. Circulating, interferon-producing plasmacytoid dendritic cells decline during human ageing. Scand J Immunol. 2002;56: 518–521. doi: 10.1046/j.1365-3083.2002.01148.x 12410802
29. Pérez-Cabezas B, Naranjo-Gómez M, Fernández MA, Grífols JR, Pujol-Borrell R, Borràs FE. Reduced numbers of plasmacytoid dendritic cells in aged blood donors. Exp Gerontol. 2007;42: 1033–1038. doi: 10.1016/j.exger.2007.05.010 17606348
30. Narbutt J, Lesiak A, Zak-Prelich M, Woźniacka A, Sysa-Jedrzejowska A, Tybura M, et al. The distribution of peripheral blood dendritic cells assayed by a new panel of anti-BDCA monoclonal antibodies in healthy representatives of the polish population. Cell Mol Biol Lett. 2004;9: 497–509. 15332126
31. Agrawal A, Agrawal S, Cao J-N, Su H, Osann K, Gupta S. Altered Innate Immune Functioning of Dendritic Cells in Elderly Humans: A Role of Phosphoinositide 3-Kinase-Signaling Pathway. J Immunol. 2007;178: 6912–6922. doi: 10.4049/jimmunol.178.11.6912 17513740
32. Della Bella S, Bierti L, Presicce P, Arienti R, Valenti M, Saresella M, et al. Peripheral blood dendritic cells and monocytes are differently regulated in the elderly. Clin Immunol. 2007;122: 220–228. doi: 10.1016/j.clim.2006.09.012 17101294
33. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, et al. Mortality Associated With Influenza and Respiratory Syncytial Virus in the United States. JAMA. 2003;289: 179–186. doi: 10.1001/jama.289.2.179 12517228
34. Rovati B, Mariucci S, Manzoni M, Bencardino K, Danova M. Flow cytometric detection of circulating dendritic cells in healthy subjects. Eur J Histochem. 2008;52: 45–52. Available: http://www.ncbi.nlm.nih.gov/pubmed/18502722 doi: 10.4081/1185 18502722
35. Piccioli D, Tavarini S, Borgogni E, Steri V, Nuti S, Sammicheli C, et al. Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood. 2007;109: 5371–5379. doi: 10.1182/blood-2006-08-038422 17332250
36. Bonafè M, Olivieri F, Cavallone L, Giovagnetti S, Marchegiani F, Cardelli M, et al. A gender–dependent genetic predisposition to produce high levels of IL-6 is detrimental for longevity Massimiliano Bonaf e. Eur J Immunol. 2001;31: 2357–2361. doi: 10.1002/1521-4141(200108)31:8<2357::aid-immu2357>3.0.co;2-x 11500818
37. Kollmann TR, Levy O, Montgomery RR, Goriely S. Innate Immune Function by Toll-like Receptors: Distinct Responses in Newborns and the Elderly. Immunity. 2012;37: 771–783. doi: 10.1016/j.immuni.2012.10.014 23159225
38. Qian F, Wan X, Zhang L, Lin A, Zhao H, Fikrig E, et al. Impaired interferon signaling in dendritic cells from older donors infected in vitro with west nile virus. J Infect Dis. 2011;203: 1415–1424. doi: 10.1093/infdis/jir048 21398396
39. Panda A, Qian F, Mohanty S, van Duin D, Newman FK, Zhang L, et al. Age-Associated Decrease in TLR Function in Primary Human Dendritic Cells Predicts Influenza Vaccine Response. J Immunol. 2010;119: 454–464. doi: 10.4049/jimmunol.0901022
40. Krug A, Rothenfusser S, Hornung V, Jahrsdrfer B, Blackwell S, Ballas ZK, et al. Identification of CpG oligonucleotide sequences with high induction of IFN-α/β in plasmacytoid dendritic cells. Eur J Immunol. 2001;31: 2154–2163. doi: 10.1002/1521-4141(200107)31:7<2154::aid-immu2154>3.0.co;2-u 11449369
41. Sirota P, Hadi E, Djaldetti M, Bessler H. Difference in inflammatory cytokine production by mononuclear cells from obese and non-obese schizophrenic patients. Acta Psychiatr Scand. 2015;132: 301–305. doi: 10.1111/acps.12396 25627461
42. Huang C, Acevedo EO, Mari DC, Randazzo C, Shibata Y. Glucocorticoid inhibition of leptin- and lipopolysaccharide-induced interleukin-6 production in obesity. Brain Behav Immun. 2014;35: 163–168. doi: 10.1016/j.bbi.2013.10.004 24126150
43. Paolisso G, Rizzo MR, Mazziotti G, Tagliamonte MR, Gambardella A, Rotondi M, et al. Advancing age and insulin resistance: role of plasma tumor necrosis factor-alpha. Am J Physiol. 1998;275: E294–9. doi: 10.1152/ajpendo.1998.275.2.E294 9688632
44. Bruunsgaard H, Andersen-Ranberg K, Jeune B, Pedersen AN, Skinhoj P, Pedersen BK. A High Plasma Concentration of TNF- Is Associated With Dementia in Centenarians. Journals Gerontol Ser A Biol Sci Med Sci. 1999;54: M357–M364. doi: 10.1093/gerona/54.7.M357 10462168
45. Ferrucci L, Corsi A, Lauretani F, Bandinelli S, Bartali B, Taub DD, et al. The origins of age-related proin ammatory state. Aging (Albany NY). 2005;105: 2294–2299. doi: 10.1182/blood-2004-07-2599.Supported
46. Kim HOS, Kim HOS, Youn JC, Shin EC, Park S. Serum cytokine profiles in healthy young and elderly population assessed using multiplexed bead-based immunoassays. J Transl Med. 2011;9: 113. doi: 10.1186/1479-5876-9-113 21774806
47. Bartlett DB, Firth CM, Phillips AC, Moss P, Baylis D, Syddall H, et al. The age-related increase in low-grade systemic inflammation (Inflammaging) is not driven by cytomegalovirus infection. Aging Cell. 2012;11: 912–915. doi: 10.1111/j.1474-9726.2012.00849.x 22708923
48. Milan-Mattos JC, Anibal FF, Perseguini NM, Minatel V, Rehder-Santos P, Castro CA, et al. Effects of natural aging and gender on pro-inflammatory markers. Brazilian J Med Biol Res. 2019;52: 1–10. doi: 10.1590/1414-431x20198392 31411315
49. Hager K, Machein U, Krieger S, Platt D, Seefried G, Bauer J. Interleukin-6 and selected plasma proteins in healthy persons of different ages. Neurobiol Aging. 1994;15: 771–772. doi: 10.1016/0197-4580(94)90066-3 7534383
50. Forsey RJ, Thompson JM, Ernerudh J, Hurst TL, Strindhall J, Johansson B, et al. Plasma cytokine profiles in elderly humans. Mech Ageing Dev. 2003;124: 487–493. doi: 10.1016/s0047-6374(03)00025-3 12714257
51. Beharka AA, Meydani M, Wu D, Leka LS, Meydani A, Meydani SN. Interleukin-6 Production Does Not Increase With Age. J Gerontol Med Sci. 2001;56: 81–88.
52. Peterson PK, Chao CC, Carson P, Hu S, Nichol K, Janoff EN. Levels of Tumor Necrosis Factor, Interleukin 6, Interleukin 10, and Transforming Growth Factor Are Normal in the Serum of the Healthy Elderly. Clin Infect Dis. 1994;19: 1158–1159. doi: 10.1093/clinids/19.6.1158 7888553
53. Catania A, Airaghi L, Motta P, Manfredi MG, Annoni G, Pettenati C, et al. Cytokine antagonists in aged subjects and their relation with cellular immunity. J Gerontol. 1997;52: B93–7. Available: http://www.ncbi.nlm.nih.gov/pubmed/9060965
54. Roubenoff R, Harris TB, Abad LW, Wilson PWF, Dallal GE, Dinarello CA. Monocyte Cytokine Production in an Elderly Population: Effect of Age and Inflammation. Journals Gerontol Ser A Biol Sci Med Sci. 1998;53A: M20–M26. doi: 10.1093/gerona/53A.1.M20 9467429
55. Kollman T, Levy O, Montgomery RR, Goriely S. Innate immune sensing by Toll-file://wurnet.nl/Homes/splun001/AppData/FolderRedirection/Desktop/160922 Kickoff MOSAIC-2 NIZO-HN-WUR (3).docxlike Receptors in newborns and the elderly. Immunity. 2012;37: 771–783. doi: 10.1016/j.immuni.2012.10.014 23159225
56. Giefing-Kröll C, Berger P, Lepperdinger G, Grubeck-Loebenstein B. How sex and age affect immune responses, susceptibility to infections, and response to vaccination. Aging Cell. 2015;14: 309–321. doi: 10.1111/acel.12326 25720438
57. Richter V, Rassoul F, Purschwitz K, Hentschel B, Reuter W, Kuntze T. Circulating vascular cell adhesion molecules VCAM-1, ICAM-1, and E-selectin in dependence on aging. Gerontology. 2003;49: 293–300. doi: 10.1159/000071710 12920349
58. Miles EA, Thies F, Wallace FA, Powell JR, Hurst TL, Newsholme EA, et al. Influence of age and dietary fish oil on plasma soluble adhesion molecule concentrations. Clin Sci. 2001;100: 91–100. doi: 10.1042/CS20000198 11115423
59. Goudev A, Kyurkchiev S, Gergova V, Karshelova E, Georgiev D, Atar D, et al. Reduced Concentrations of Soluble Adhesion Molecules after Antioxidant Supplementation in Postmenopausal Women with High Cardiovascular Risk Profiles–A Randomized Double-Blind Study. Cardiology. 2000;94: 227–232. doi: 10.1159/000047322 11326143
60. Olivieri F, Rippo MR, Monsurrò V, Salvioli S, Capri M, Procopio AD, et al. MicroRNAs linking inflamm-aging, cellular senescence and cancer. Ageing Res Rev. 2013;12: 1056–1068. doi: 10.1016/j.arr.2013.05.001 23688930
61. Olivieri F, Capri M, Morsiani C, Jung HJ, Spazzafumo L, Viña J, et al. Circulating miRNAs and miRNA shuttles as biomarkers: Perspective trajectories of healthy and unhealthy aging. Mech Ageing Dev. 2017;165: 162–170. doi: 10.1016/j.mad.2016.12.004 27986629
62. Kangas R, Pöllänen E, Rippo MR, Lanzarini C, Prattichizzo F, Niskala P, et al. Circulating miR-21, miR-146a and Fas ligand respond to postmenopausal estrogen-based hormone replacement therapy—A study with monozygotic twin pairs. Mech Ageing Dev. 2014;143–144: 1–8. doi: 10.1016/j.mad.2014.11.001 25448133
63. Guerra-Silveira F, Abad-Franch F. Sex Bias in Infectious Disease Epidemiology: Patterns and Processes. PLoS One. 2013;8. doi: 10.1371/journal.pone.0062390 23638062
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