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Published in: Immunity & Ageing 1/2017

Open Access 01-12-2017 | Research

Changes in peripheral immune cell numbers and functions in octogenarian walkers – an acute exercise study

Authors: Kornelis S. M. van der Geest, Qi Wang, Thijs M. H. Eijsvogels, Hans J. P. Koenen, Irma Joosten, Elisabeth Brouwer, Maria T. E. Hopman, Joannes F. M. Jacobs, Annemieke M. H. Boots

Published in: Immunity & Ageing | Issue 1/2017

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Abstract

Background

Age-related changes of the immune system, termed immunosenescence, may underlie the increased risk of infections and morbidity in the elderly. Little is known about the effects of acute exercise on peripheral immune parameters in octogenarians. Therefore, we investigated acute exercise-induced changes in phenotype and function of the immune system in octogenarians participating in the 2013 edition of the Nijmegen Four Days Marches. Blood sampling was performed at baseline and immediately after 4 days of the walking exercise (30 km/day). A comprehensive set of adaptive and innate immune traits were enumerated and analyzed by flow-cytometry. Peripheral blood mononuclear cells, isolated before and after walking were stimulated with LPS and supernatants were analysed for IL-1β, IL-6, IL-8 and TNF-α concentrations by ELISA. CMV serostatus was determined by ELISA.

Results

The walking exercise induced a clear leucocytosis with numerical increases of granulocytes, monocytes and lymphocytes. These exercise-induced changes were most profound in CMV seropositive subjects. Within lymphocytes, numerical increases of particularly CD4+ T cells were noted. Further T cell differentiation analysis revealed profound increases of naïve CD4+ T cells, including naïve Treg. Significant increases were also noted for CD4+ memory T cell subsets. In contrast, only slight increases in naïve and memory CD8+ T cell subsets were detected. Exercise did not affect markers of immune exhaustion in memory T cell subsets. NK cells demonstrated a numerical decline and a change in cellular composition with a selective decrease of the mature CD56dim NK cells. The latter was seen in CMV seronegative subjects only. Also, a higher IL-6 and IL-8 production capacity of LPS-stimulated PBMC was seen after walking.

Conclusion

In this exceptional cohort of octogenarian walkers, acute exercise induced changes in immune cell numbers and functions. A clear response of CD4+ T cells, rather than CD8+ T cells or NK cells was noted. Remarkably, the response to exercise within the CD4+ T cell compartment was dominated by naïve CD4+ subsets.
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Literature
1.
go back to reference Fulop T, Kotb R, Fortin CF, Pawelec G, de Angelis F, Larbi A. Potential role of immunosenescence in cancer development. Ann N Y Acad Sci. 2010;1197(1):158.CrossRefPubMed Fulop T, Kotb R, Fortin CF, Pawelec G, de Angelis F, Larbi A. Potential role of immunosenescence in cancer development. Ann N Y Acad Sci. 2010;1197(1):158.CrossRefPubMed
2.
go back to reference Poland GA, Ovsyannikova IG, Kennedy RB, Lambert ND, Kirkland JL. A systems biology approach to the effect of aging, immunosenescence and vaccine response. Curr Opin Immunol. 2014;29:62.CrossRefPubMed Poland GA, Ovsyannikova IG, Kennedy RB, Lambert ND, Kirkland JL. A systems biology approach to the effect of aging, immunosenescence and vaccine response. Curr Opin Immunol. 2014;29:62.CrossRefPubMed
3.
go back to reference Yoshikawa TT. Epidemiology and unique aspects of aging and infectious diseases. Clin Infect Dis. 2000;30(6):931.CrossRefPubMed Yoshikawa TT. Epidemiology and unique aspects of aging and infectious diseases. Clin Infect Dis. 2000;30(6):931.CrossRefPubMed
4.
6.
go back to reference Weltevrede M, Eilers R, de Melker HE, van Baarle D. Cytomegalovirus persistence and T-cell immunosenescence in people aged fifty and older: A systematic review. Exp Gerontol. 2016;77:87–95.CrossRefPubMed Weltevrede M, Eilers R, de Melker HE, van Baarle D. Cytomegalovirus persistence and T-cell immunosenescence in people aged fifty and older: A systematic review. Exp Gerontol. 2016;77:87–95.CrossRefPubMed
7.
go back to reference van der Geest KS, Abdulahad WH, Horst G, et al. Quantifying Distribution of Flow Cytometric TCR-Vbeta Usage with Economic Statistics. PloS One. 2015a;10(4):e0125373. van der Geest KS, Abdulahad WH, Horst G, et al. Quantifying Distribution of Flow Cytometric TCR-Vbeta Usage with Economic Statistics. PloS One. 2015a;10(4):e0125373.
8.
go back to reference Akbar AN, Henson SM. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol. 2011;11(4):289.CrossRefPubMed Akbar AN, Henson SM. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol. 2011;11(4):289.CrossRefPubMed
9.
go back to reference van der Geest KSM, Abdulahad WH, Tete SM, et al. Ageing disturbs the balance between effector and regulatory CD4+ T cells. Exp Gerontol. 2014;60:190.CrossRefPubMed van der Geest KSM, Abdulahad WH, Tete SM, et al. Ageing disturbs the balance between effector and regulatory CD4+ T cells. Exp Gerontol. 2014;60:190.CrossRefPubMed
10.
go back to reference Booth NJ, McQuaid AJ, Sobande T, et al. Different proliferative potential and migratory characteristics of human CD4+ regulatory T cells that express either CD45RA or CD45RO. J Immunol. 2010;184:4317.CrossRefPubMed Booth NJ, McQuaid AJ, Sobande T, et al. Different proliferative potential and migratory characteristics of human CD4+ regulatory T cells that express either CD45RA or CD45RO. J Immunol. 2010;184:4317.CrossRefPubMed
13.
go back to reference Franceschi C, Capri M, Monti D, et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128(1):92.CrossRefPubMed Franceschi C, Capri M, Monti D, et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128(1):92.CrossRefPubMed
14.
go back to reference Biagi E, Nylund L, Candela M, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 2010;5(5):e10667.CrossRefPubMedPubMedCentral Biagi E, Nylund L, Candela M, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 2010;5(5):e10667.CrossRefPubMedPubMedCentral
15.
go back to reference Solana R, Campos C, Pera A, Tarazona R. Shaping of NK cell subsets by aging. Curr Opin Immunol. 2014;29:56.CrossRefPubMed Solana R, Campos C, Pera A, Tarazona R. Shaping of NK cell subsets by aging. Curr Opin Immunol. 2014;29:56.CrossRefPubMed
16.
go back to reference Walsh NP, Gleeson M, Shephard RJ, et al. Position Statement. Part one: Immune function and exercise. Exerc Immunol Rev. 2011;17:6–63.PubMed Walsh NP, Gleeson M, Shephard RJ, et al. Position Statement. Part one: Immune function and exercise. Exerc Immunol Rev. 2011;17:6–63.PubMed
17.
18.
go back to reference Simpson RJ, Bosch JA. Special issue on exercise immunology: current perspectives on aging, health and extreme performance. Brain Behav Immun. 2014;39:1.CrossRefPubMed Simpson RJ, Bosch JA. Special issue on exercise immunology: current perspectives on aging, health and extreme performance. Brain Behav Immun. 2014;39:1.CrossRefPubMed
19.
go back to reference Bigley AB, Rezvani K, Chew C, et al. Acute exercise preferentially redeploys NK-cells with a highly-differentiated phenotype and augments cytotoxicity against lymphoma and multiple myeloma target cells. Brain Behav Immun. 2014;39:160.CrossRefPubMed Bigley AB, Rezvani K, Chew C, et al. Acute exercise preferentially redeploys NK-cells with a highly-differentiated phenotype and augments cytotoxicity against lymphoma and multiple myeloma target cells. Brain Behav Immun. 2014;39:160.CrossRefPubMed
20.
go back to reference Campbell JP, Riddell NE, Burns VE, et al. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effector-memory phenotype. Brain Behav Immun. 2009;6:767.CrossRef Campbell JP, Riddell NE, Burns VE, et al. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effector-memory phenotype. Brain Behav Immun. 2009;6:767.CrossRef
21.
go back to reference Turner JE, Aldred S, Witard OC. Latent Cytomegalovirus infection amplifies CD8 T-lymphocyte mobilisation and egress in response to exercise. Brain Behav Immun. 2010;24:1362.CrossRefPubMed Turner JE, Aldred S, Witard OC. Latent Cytomegalovirus infection amplifies CD8 T-lymphocyte mobilisation and egress in response to exercise. Brain Behav Immun. 2010;24:1362.CrossRefPubMed
22.
go back to reference Simpson RJ, Bigley AB, Spielmann G, et al. Human cytomegalovirus infection and the immune response to exercise. Exerc Immunol Rev. 2016;22:8.PubMed Simpson RJ, Bigley AB, Spielmann G, et al. Human cytomegalovirus infection and the immune response to exercise. Exerc Immunol Rev. 2016;22:8.PubMed
23.
go back to reference Jacobs JF, Eijsvogels TM, van der Geest KS, et al. The impact of exercise on the variation of serum free light chains. Clin Chem Lab Med. 2014;52(11):e239.PubMed Jacobs JF, Eijsvogels TM, van der Geest KS, et al. The impact of exercise on the variation of serum free light chains. Clin Chem Lab Med. 2014;52(11):e239.PubMed
24.
go back to reference Eijsvogels TM, Veltmeijer MT, George K, Hopman MT, Thijssen DH. The impact of obesity on cardiac troponin levels after prolonged exercise in humans. Eur J Appl Physiol. 2012;112(5):1725.CrossRefPubMed Eijsvogels TM, Veltmeijer MT, George K, Hopman MT, Thijssen DH. The impact of obesity on cardiac troponin levels after prolonged exercise in humans. Eur J Appl Physiol. 2012;112(5):1725.CrossRefPubMed
25.
go back to reference Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol. 2001;37:153.CrossRefPubMed Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol. 2001;37:153.CrossRefPubMed
26.
go back to reference Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr. 1974;32(1):77.CrossRefPubMed Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr. 1974;32(1):77.CrossRefPubMed
27.
go back to reference Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol. 1974;37(2):247.PubMed Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol. 1974;37(2):247.PubMed
28.
go back to reference Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol. 2004;22:745.CrossRefPubMed Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol. 2004;22:745.CrossRefPubMed
29.
go back to reference Kimmig S, Przybylski GK, Schmidt CA, et al. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J Exp Med. 2002;195:789.CrossRefPubMedPubMedCentral Kimmig S, Przybylski GK, Schmidt CA, et al. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J Exp Med. 2002;195:789.CrossRefPubMedPubMedCentral
30.
go back to reference van der Geest KS, Abdulahad WH, Teteloshvili N, et al. Low-affinity TCR engagement drives IL-2-dependent post-thymic maintenance of naive CD4+ T cells in aged humans. Aging Cell. 2015;14(5):744.CrossRefPubMedPubMedCentral van der Geest KS, Abdulahad WH, Teteloshvili N, et al. Low-affinity TCR engagement drives IL-2-dependent post-thymic maintenance of naive CD4+ T cells in aged humans. Aging Cell. 2015;14(5):744.CrossRefPubMedPubMedCentral
31.
go back to reference Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30:899.CrossRefPubMed Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30:899.CrossRefPubMed
32.
go back to reference Spielmann G, Bollard CM, Bigley AB, et al. The effects of age and latent cytomegalovirus infection on the redeployment of CD8+ T cell subsets in response to acute exercise in humans. Brain Behav Immun. 2014;39:142.CrossRefPubMed Spielmann G, Bollard CM, Bigley AB, et al. The effects of age and latent cytomegalovirus infection on the redeployment of CD8+ T cell subsets in response to acute exercise in humans. Brain Behav Immun. 2014;39:142.CrossRefPubMed
33.
go back to reference Bigley AB, Spielmann G, Agha N, Simpson RJ. The effects of age and latent Cytomegalovirus infection on NK-cell phenotype and exercise responsiveness in man. Oxid Med Cell Longev. 2015;2015:979645.CrossRefPubMedPubMedCentral Bigley AB, Spielmann G, Agha N, Simpson RJ. The effects of age and latent Cytomegalovirus infection on NK-cell phenotype and exercise responsiveness in man. Oxid Med Cell Longev. 2015;2015:979645.CrossRefPubMedPubMedCentral
34.
go back to reference Bigley AB, Rezvani K, Pistillo M, et al. Acute exercise preferentially redeploys NK-cells with a highly-differentiated phenotype and augments cytotoxicity against lymphoma and multiple myeloma target cells. Part II: impact of latent cytomegalovirus infection and catecholamine sensitivity. Brain Behav Immun. 2015;49:59.CrossRefPubMed Bigley AB, Rezvani K, Pistillo M, et al. Acute exercise preferentially redeploys NK-cells with a highly-differentiated phenotype and augments cytotoxicity against lymphoma and multiple myeloma target cells. Part II: impact of latent cytomegalovirus infection and catecholamine sensitivity. Brain Behav Immun. 2015;49:59.CrossRefPubMed
36.
go back to reference Nikolich-Zugich J, Slifka MK, Messaoudi I. The many important facets of T-cell repertoire diversity. Nat Rev Immunol. 2004;4(2):123.CrossRefPubMed Nikolich-Zugich J, Slifka MK, Messaoudi I. The many important facets of T-cell repertoire diversity. Nat Rev Immunol. 2004;4(2):123.CrossRefPubMed
39.
go back to reference Wertheimer AM, Bennett MS, Park B, et al. Aging and cytomegalovirus infection differentially and jointly affect distinct circulating T cell subsets in humans. J Immunol. 2014;192:2143.CrossRefPubMedPubMedCentral Wertheimer AM, Bennett MS, Park B, et al. Aging and cytomegalovirus infection differentially and jointly affect distinct circulating T cell subsets in humans. J Immunol. 2014;192:2143.CrossRefPubMedPubMedCentral
40.
go back to reference den Braber I, Mugwagwa T, Vrisekoop N, et al. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity. 2012;36:288.CrossRef den Braber I, Mugwagwa T, Vrisekoop N, et al. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity. 2012;36:288.CrossRef
41.
go back to reference Pekalski ML, Ferreira RC, Coulson RM, et al. Postthymic Expansion in Human CD4 Naive T Cells Defined by Expression of Functional High-Affinity IL-2 Receptors. J Immunol. 2013;190:2554.CrossRefPubMedPubMedCentral Pekalski ML, Ferreira RC, Coulson RM, et al. Postthymic Expansion in Human CD4 Naive T Cells Defined by Expression of Functional High-Affinity IL-2 Receptors. J Immunol. 2013;190:2554.CrossRefPubMedPubMedCentral
42.
go back to reference Thome JJ, Bickham KL, Ohmura Y, et al. Early-life compartmentalization of human T cell differentiation and regulatory function in mucosal and lymphoid tissues. Nat Med. 2016;22(1):72.CrossRefPubMed Thome JJ, Bickham KL, Ohmura Y, et al. Early-life compartmentalization of human T cell differentiation and regulatory function in mucosal and lymphoid tissues. Nat Med. 2016;22(1):72.CrossRefPubMed
Metadata
Title
Changes in peripheral immune cell numbers and functions in octogenarian walkers – an acute exercise study
Authors
Kornelis S. M. van der Geest
Qi Wang
Thijs M. H. Eijsvogels
Hans J. P. Koenen
Irma Joosten
Elisabeth Brouwer
Maria T. E. Hopman
Joannes F. M. Jacobs
Annemieke M. H. Boots
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Immunity & Ageing / Issue 1/2017
Electronic ISSN: 1742-4933
DOI
https://doi.org/10.1186/s12979-017-0087-2

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