12-week combined strength and endurance exercise attenuates CD8 <sup>+</sup> T-cell differentiation and affects the kynurenine pathway in the elderly: a randomized controlled trial

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Abstract

Background

Age-related accumulation of highly differentiated CD8 ⁺ effector memory re-expressing CD45RA (EMRA) T-cells and disruption of the kynurenine (KYN) pathway are associated with chronic inflammation and the development of insulin resistance.

In this study the aim was to investigate the effects of 12-week combined strength and endurance exercise on CD8 ⁺ T-cell differentiation and KYN pathway metabolites. Ninety-six elderly subjects (f/m, aged 50—70) were randomized to a control (CON) or exercise (EX) group. The EX group completed combined strength and endurance training twice weekly for one hour each time at an intensity of 60% of the one-repetition maximum for strength exercises and a perceived exertion of 15/20 for endurance exercises. The EX group was also randomly subdivided into two groups with or without a concomitant balanced diet intervention in order to examine additional effects besides exercise alone. Before and after the intervention phase, the proportions of CD8 ⁺ T-cell subsets and levels of KYN pathway metabolites in peripheral blood were determined.

Results

The CD8 ⁺ EMRA T-cell subsets increased in the CON group but remained almost unchanged in the EX group ( p = .02). Plasma levels of kynurenic acid (KA) increased in the EX group and decreased in the CON group ( p = .03). Concomitant nutritional intervention resulted in lower levels of quinolinic acid (QA) compared with exercise alone ( p = .03). Overall, there was a slight increase in the QA/KA ratio in the CON group, whereas it decreased in the EX group ( p > .05).

Conclusions

Combined strength and endurance training seems to be a suitable approach to attenuate CD8 ⁺ T-cell differentiation in the elderly and to redirect the KYN pathway towards KA. The clinical relevance of these effects needs further investigation.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12979-023-00347-7.

Related collections

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The aryl hydrocarbon receptor (AHR) has been known to cause immunosuppression after binding dioxin. It has recently been discovered that the receptor may be central to T cell differentiation into FoxP3(+) regulatory T cells (Tregs) versus Th17 cells. In this paper, we demonstrate that kynurenine, the first breakdown product in the IDO-dependent tryptophan degradation pathway, activates the AHR. We furthermore show that this activation leads to AHR-dependent Treg generation. We additionally investigate the dependence of TGF-beta on the AHR for optimal Treg generation, which may be secondary to the upregulation of this receptor that is seen in T cells postexposure to TGF-beta. These results shed light on the relationship of IDO to the generation of Tregs, in addition to highlighting the central importance of the AHR in T cell differentiation. All tissues and cells were derived from mice.

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Author and article information

Contributors

Tim Konstantin Boßlau: tim.k.bosslau@med.uni-giessen.de

Paulina Wasserfurth: paulina.wasserfurth@tum.de

Thomas Reichel: thomas.reichel@sport.uni-giessen.de

Christopher Weyh: christopher.weyh@sport.uni-giessen.de

Jana Palmowski: jana.palmowski@sport.uni-giessen.de

Josefine Nebl: josefine_nebl@web.de

Niklas Joisten: niklas.joisten@tu-dortmund.de

Sergen Belen: sergen.belen@tu-dortmund.de

Alexander Schenk: alexander.schenk@tu-dortmund.de

Andreas Hahn: hahn@nutrition.uni-hannover.de

Philipp Zimmer: philipp.zimmer@tu-dortmund.de

Karsten Krüger: karsten.krueger@sport.uni-giessen.de

Journal

Journal ID (nlm-ta): Immun Ageing

Journal ID (iso-abbrev): Immun Ageing

Title: Immunity & Ageing : I & A

Publisher: BioMed Central (London )

ISSN (Electronic): 1742-4933

Publication date (Electronic): 9 May 2023

Publication date PMC-release: 9 May 2023

Publication date Collection: 2023

Volume: 20

Electronic Location Identifier: 19

Affiliations

[1 ]GRID grid.8664.c, ISNI 0000 0001 2165 8627, Department of Exercise Physiology and Sports Therapy, Institute of Sports Science, , Justus-Liebig-University Giessen, ; Kugelberg 62, 35394 Giessen, Germany

[2 ]GRID grid.6936.a, ISNI 0000000123222966, Department of Exercise, Nutrition and Health, Faculty of Sport and Health Sciences, , Technical University Munich, ; Connollystraße 32, 80809 Munich, Germany

[3 ]GRID grid.9122.8, ISNI 0000 0001 2163 2777, Faculty of Natural Sciences, Institute of Food Science and Human Nutrition, , Leibniz University Hanover, ; Am Kleinen Felde 30, 30159 Hannover, Germany

[4 ]GRID grid.5675.1, ISNI 0000 0001 0416 9637, Division of Performance and Health, Institute for Sport and Sport Science, , Technical University Dortmund, ; Otto-Hahn-Str. 3, 44227 Dortmund, Germany

Article

Publisher ID: 347

DOI: 10.1186/s12979-023-00347-7

PMC ID: 10169370

SO-VID: 327bc9d5-62fa-4765-a16c-8ba2c2005ae4

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 24 September 2022

Date accepted : 3 May 2023

Funding

Funded by: Justus-Liebig-Universität Gießen (3114)

Open Access :

Open Access funding enabled and organized by Projekt DEAL.

Custom metadata

ScienceOpen disciplines: Immunology

Keywords: ageing,cd8+ emra t-cells,kynurenine pathway,exercise,nutrition,insulin resistance

Data availability:

ScienceOpen disciplines: Immunology

Keywords: ageing, cd8+ emra t-cells, kynurenine pathway, exercise, nutrition, insulin resistance