Skip to main content
Top
Published in: Immunologic Research 5/2017

01-10-2017 | Original Article

Age-dependent alterations in serum cytokines, peripheral blood mononuclear cell cytokine production, natural killer cell activity, and prostaglandin F

Authors: Dong Hee Lee, Minkyung Kim, Minjoo Kim, Young Ju Lee, Hye Jin Yoo, Sang-Hyun Lee, Jong Ho Lee

Published in: Immunologic Research | Issue 5/2017

Login to get access

Abstract

This study aimed to determine age-dependent alterations in serum cytokines, peripheral blood mononuclear cell (PBMC) cytokine production, natural killer (NK) cell activity, and urinary 8-epi-prostaglandin F (PGF). Nine hundred eighty-seven healthy and nonobese subjects were divided into five age groups: 20–34 (group 1), 35–44 (group 2), 45–54 (group 3), 55–64 (group 4), and 65–80 (group 5) years of age. After adjusting for BMI, sex, and smoking and drinking status, serum interferon (IFN)-γ levels decreased in groups 3, 4, and 5 compared with those in groups 1 and 2. Production of IFN-γ by unstimulated PBMCs was lower in the older groups (groups 4 and 5) than in the younger groups (groups 1 and 3). Serum interleukin (IL)-12 was lower in group 5 than in groups 1 and 2. In contrast, both serum and PBMC IL-6 were higher in group 5 than in groups 1, 2, and 3. Urinary 8-epi-PGF increased in group 3 compared with that in group 1 and further increased in group 5. Multiple linear regression analysis revealed that serum IFN-γ levels were negatively affected by age, and NK cell activity at a ratio of E:T = 5:1 was positively affected by PBMC IFN-γ. This study shows the age-related reductions in serum and PBMC IFN-γ and serum IL-12 and age-related increases in serum and PBMC IL-6 and oxidative stress in healthy nonobese subjects. Additionally, circulating IL-6 levels may be a better marker of the chronic low-grade inflammatory activity associated with aging than systemic levels of high-sensitivity C-reactive protein, TNF-α, and IL-1β.
Literature
1.
go back to reference Welzl K, Kern G, Mayer G, Weinberger B, Säemann MD, Sturm G, et al. Effect of different immunosuppressive drugs on immune cells from young and old healthy persons. Gerontology. 2014;60:229–38. Welzl K, Kern G, Mayer G, Weinberger B, Säemann MD, Sturm G, et al. Effect of different immunosuppressive drugs on immune cells from young and old healthy persons. Gerontology. 2014;60:229–38.
2.
go back to reference Lessiani G, Santilli F, Boccatonda A, Iodice P, Liani R, Tripaldi R, et al. Arterial stiffness and sedentary lifestyle: role of oxidative stress. Vasc Pharmacol. 2016;79:1–5. Lessiani G, Santilli F, Boccatonda A, Iodice P, Liani R, Tripaldi R, et al. Arterial stiffness and sedentary lifestyle: role of oxidative stress. Vasc Pharmacol. 2016;79:1–5.
3.
go back to reference Alvarez-Rodríguez L, López-Hoyos M, Muñoz-Cacho P, Martínez-Taboada VM. Aging is associated with circulating cytokine dysregulation. Cell Immunol. 2012;273:124–32.CrossRefPubMed Alvarez-Rodríguez L, López-Hoyos M, Muñoz-Cacho P, Martínez-Taboada VM. Aging is associated with circulating cytokine dysregulation. Cell Immunol. 2012;273:124–32.CrossRefPubMed
4.
go back to reference Krause D, Mastro AM, Handte G, Smiciklas-Wright H, Miles MP, Ahluwalia N. Immune function did not decline with aging in apparently healthy, well-nourished women. Mech Ageing Dev. 1999;112:43–57.CrossRefPubMed Krause D, Mastro AM, Handte G, Smiciklas-Wright H, Miles MP, Ahluwalia N. Immune function did not decline with aging in apparently healthy, well-nourished women. Mech Ageing Dev. 1999;112:43–57.CrossRefPubMed
5.
go back to reference Paik JK, Chae JS, Kang R, Kwon N, Lee SH, Lee JH. Effect of age on atherogenicity of LDL and inflammatory markers in healthy women. Nutr Metab Cardiovasc Dis. 2013;23:967–72.CrossRefPubMed Paik JK, Chae JS, Kang R, Kwon N, Lee SH, Lee JH. Effect of age on atherogenicity of LDL and inflammatory markers in healthy women. Nutr Metab Cardiovasc Dis. 2013;23:967–72.CrossRefPubMed
6.
go back to reference Kim OY, Chae JS, Paik JK, Seo HS, Jang Y, Cavaillon JM, et al. Effects of aging and menopause on serum interleukin-6 levels and peripheral blood mononuclear cell cytokine production in healthy nonobese women. Age. 2012;34:415–25. Kim OY, Chae JS, Paik JK, Seo HS, Jang Y, Cavaillon JM, et al. Effects of aging and menopause on serum interleukin-6 levels and peripheral blood mononuclear cell cytokine production in healthy nonobese women. Age. 2012;34:415–25.
7.
go back to reference Ahluwalia N, Mastro AM, Ball R, Miles MP, Rajendra R, Handte G. Cytokine production by stimulated mononuclear cells did not change with aging in apparently healthy, well-nourished women. Mech Ageing Dev. 2001;122:1269–79.CrossRefPubMed Ahluwalia N, Mastro AM, Ball R, Miles MP, Rajendra R, Handte G. Cytokine production by stimulated mononuclear cells did not change with aging in apparently healthy, well-nourished women. Mech Ageing Dev. 2001;122:1269–79.CrossRefPubMed
8.
go back to reference Heremans H, Dillen C, van Damme J, Billiau A. Essential role for natural killer cells in the lethal lipopolysaccharide-induced Shwartzman-like reaction in mice. Eur J Immunol. 1994;24:1155–60.CrossRefPubMed Heremans H, Dillen C, van Damme J, Billiau A. Essential role for natural killer cells in the lethal lipopolysaccharide-induced Shwartzman-like reaction in mice. Eur J Immunol. 1994;24:1155–60.CrossRefPubMed
9.
go back to reference Roy S, Pavitrakar D, Gunjikar R, Ayachit VM, Bondre VP, Sapkal GN. Monocytes and B cells support active replication of Chandipura virus. BMC Infect Dis. 2016;16:487.CrossRefPubMedPubMedCentral Roy S, Pavitrakar D, Gunjikar R, Ayachit VM, Bondre VP, Sapkal GN. Monocytes and B cells support active replication of Chandipura virus. BMC Infect Dis. 2016;16:487.CrossRefPubMedPubMedCentral
10.
go back to reference Solana R, Alonso MC, Peña J. Natural killer cells in healthy aging. Exp Gerontol. 1999;34:435–43.CrossRefPubMed Solana R, Alonso MC, Peña J. Natural killer cells in healthy aging. Exp Gerontol. 1999;34:435–43.CrossRefPubMed
11.
12.
go back to reference Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E. Natural-killer cells and dendritic cells: “l'union fait la force”. Blood. 2015;106:2252–8.CrossRef Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E. Natural-killer cells and dendritic cells: “l'union fait la force”. Blood. 2015;106:2252–8.CrossRef
13.
go back to reference Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR, et al. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol. 2009;30:325–33. Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR, et al. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol. 2009;30:325–33.
14.
go back to reference Nogusa S, Murasko DM, Gardner EM. Differential effects of stimulatory factors on natural killer cell activities of young and aged mice. J Gerontol A Biol Sci Med Sci. 2012;67:947–54.CrossRefPubMedPubMedCentral Nogusa S, Murasko DM, Gardner EM. Differential effects of stimulatory factors on natural killer cell activities of young and aged mice. J Gerontol A Biol Sci Med Sci. 2012;67:947–54.CrossRefPubMedPubMedCentral
15.
go back to reference Zhang Y, Wang Y, Gilmore X, Xu K, Mbawuike IN. Independent and synergistic effects of interleukin-18 and interleukin-12 in augmenting cytotoxic T lymphocyte responses and IFN-gamma production in aging. J Interf Cytokine Res. 2001;21:843–50.CrossRef Zhang Y, Wang Y, Gilmore X, Xu K, Mbawuike IN. Independent and synergistic effects of interleukin-18 and interleukin-12 in augmenting cytotoxic T lymphocyte responses and IFN-gamma production in aging. J Interf Cytokine Res. 2001;21:843–50.CrossRef
16.
go back to reference Nair MP, Kandaswami C, Mahajan S, Chadha KC, Chawda R, Nair H, et al. The flavonoid, quercetin, differentially regulates Th-1 (IFNgamma) and Th-2 (IL4) cytokine gene expression by normal peripheral blood mononuclear cells. Biochim Biophys Acta. 2002;1593:29–36. Nair MP, Kandaswami C, Mahajan S, Chadha KC, Chawda R, Nair H, et al. The flavonoid, quercetin, differentially regulates Th-1 (IFNgamma) and Th-2 (IL4) cytokine gene expression by normal peripheral blood mononuclear cells. Biochim Biophys Acta. 2002;1593:29–36.
17.
go back to reference Tousoulis D, Oikonomou E, Economou EK, Crea F, Kaski JC. Inflammatory cytokines in atherosclerosis: current therapeutic approaches. Eur Heart J. 2016;37:1723–32.CrossRefPubMed Tousoulis D, Oikonomou E, Economou EK, Crea F, Kaski JC. Inflammatory cytokines in atherosclerosis: current therapeutic approaches. Eur Heart J. 2016;37:1723–32.CrossRefPubMed
18.
go back to reference Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflammatory cytokines. Curr Opin Hematol. 2001;8:131–6.CrossRefPubMed Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflammatory cytokines. Curr Opin Hematol. 2001;8:131–6.CrossRefPubMed
19.
go back to reference Martocchia A, Stefanelli M, Falaschi GM, Toussan L, Ferri C, Falaschi P. Recent advances in the role of cortisol and metabolic syndrome in age-related degenerative diseases. Aging Clin Exp Res. 2016;28:17–23.CrossRefPubMed Martocchia A, Stefanelli M, Falaschi GM, Toussan L, Ferri C, Falaschi P. Recent advances in the role of cortisol and metabolic syndrome in age-related degenerative diseases. Aging Clin Exp Res. 2016;28:17–23.CrossRefPubMed
20.
go back to reference Lahousse L, Moyse E, Krantic S, Brusselle GG. Understanding age-related diseases: report of the 2015 ageing summit. Eur Respir J. 2016;47:5–9.CrossRefPubMed Lahousse L, Moyse E, Krantic S, Brusselle GG. Understanding age-related diseases: report of the 2015 ageing summit. Eur Respir J. 2016;47:5–9.CrossRefPubMed
21.
go back to reference Barnes PJ. Mechanisms of development of multimorbidity in the elderly. Eur Respir J. 2015;45:790–806.CrossRefPubMed Barnes PJ. Mechanisms of development of multimorbidity in the elderly. Eur Respir J. 2015;45:790–806.CrossRefPubMed
22.
go back to reference Singh U, Devaraj S, Jialal I. Vitamin E, oxidative stress, and inflammation. Annu Rev Nutr. 2005;25:151–74.CrossRefPubMed Singh U, Devaraj S, Jialal I. Vitamin E, oxidative stress, and inflammation. Annu Rev Nutr. 2005;25:151–74.CrossRefPubMed
23.
go back to reference Shoelson SE, Lee J, Yuan M. Inflammation and the IKK beta/I kappa B/NF-kappa B axis in obesity- and diet-induced insulin resistance. Int J Obes Relat Metab Disord. 2003;27:S49–52.CrossRefPubMed Shoelson SE, Lee J, Yuan M. Inflammation and the IKK beta/I kappa B/NF-kappa B axis in obesity- and diet-induced insulin resistance. Int J Obes Relat Metab Disord. 2003;27:S49–52.CrossRefPubMed
24.
go back to reference Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer. 2007;121:2381–6.CrossRefPubMed Federico A, Morgillo F, Tuccillo C, Ciardiello F, Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int J Cancer. 2007;121:2381–6.CrossRefPubMed
25.
go back to reference Roberts LJ, Morrow JD. Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo. Free Radic Biol Med. 2000;28:505–13.CrossRefPubMed Roberts LJ, Morrow JD. Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo. Free Radic Biol Med. 2000;28:505–13.CrossRefPubMed
Metadata
Title
Age-dependent alterations in serum cytokines, peripheral blood mononuclear cell cytokine production, natural killer cell activity, and prostaglandin F2α
Authors
Dong Hee Lee
Minkyung Kim
Minjoo Kim
Young Ju Lee
Hye Jin Yoo
Sang-Hyun Lee
Jong Ho Lee
Publication date
01-10-2017
Publisher
Springer US
Published in
Immunologic Research / Issue 5/2017
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-017-8940-0

Other articles of this Issue 5/2017

Immunologic Research 5/2017 Go to the issue