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Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans

BACKGROUND: Progressive age-associated change in frequencies and functional capacities of immune cells is known as immunosenescence. Despite data linking chronic environmental, physiological, and psychosocial stressors with accelerated aging, how stress contributes to immunosenesence is not well cha...

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Autores principales: Snodgrass, Ryan G., Jiang, Xiaowen, Stephensen, Charles B., Laugero, Kevin D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288764/
https://www.ncbi.nlm.nih.gov/pubmed/37353855
http://dx.doi.org/10.1186/s12979-023-00357-5
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author Snodgrass, Ryan G.
Jiang, Xiaowen
Stephensen, Charles B.
Laugero, Kevin D.
author_facet Snodgrass, Ryan G.
Jiang, Xiaowen
Stephensen, Charles B.
Laugero, Kevin D.
author_sort Snodgrass, Ryan G.
collection PubMed
description BACKGROUND: Progressive age-associated change in frequencies and functional capacities of immune cells is known as immunosenescence. Despite data linking chronic environmental, physiological, and psychosocial stressors with accelerated aging, how stress contributes to immunosenesence is not well characterized. OBJECTIVE: To help delineate the contribution of cumulative physiological stress on immunosensence we assessed relationships between a composite measurement of cumulative physiological stress, reflecting the functioning of the hypothalamic-pituitary-adrenal axis, sympathetic nervous system, cardiovascular system, and metabolic processes, and lymphocyte changes typically affiliated with aging in a cohort of healthy volunteers ranging from 18 to 66 y. RESULTS: Physiological stress load positively correlated with subject age in the study cohort and was significantly higher in adults 50–66 y compared to adults 18–33 y and 34–49 y. Using physiological stress load, we identified a significant age-dependent association between stress load and frequencies of circulating regulatory T lymphocytes (Tregs). Frequencies were higher in younger participants, but only in participants exhibiting low physiological stress load. As stress load increased, frequencies of Tregs decreased in young participants but were unchanged with increasing stress load in middle and older age individuals. Follow-up analysis of stress load components indicated lower circulating DHEA-S and higher urinary norepinephrine as the primary contributors to the effects of total stress load on Tregs. In addition, we identified age-independent inverse associations between stress load and frequencies of naïve Tregs and naïve CD4 T cells and positive associations between stress load and frequencies of memory Tregs and memory CD4 T cells. These associations were primarily driven by stress load components waist circumference, systolic and diastolic blood pressure, CRP, and HbA1c. In summary, our study results suggest that, in younger people, physiological stress load may diminish regulatory T cell frequencies to levels seen in older persons. Furthermore, independent of age, stress load may contribute to contraction of the naïve Treg pool and accumulation of memory Treg cells. CLINICAL TRIAL: Registered on ClincialTrials.gov (Identifier: NCT02367287). SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12979-023-00357-5.
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spelling pubmed-102887642023-06-24 Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans Snodgrass, Ryan G. Jiang, Xiaowen Stephensen, Charles B. Laugero, Kevin D. Immun Ageing Research BACKGROUND: Progressive age-associated change in frequencies and functional capacities of immune cells is known as immunosenescence. Despite data linking chronic environmental, physiological, and psychosocial stressors with accelerated aging, how stress contributes to immunosenesence is not well characterized. OBJECTIVE: To help delineate the contribution of cumulative physiological stress on immunosensence we assessed relationships between a composite measurement of cumulative physiological stress, reflecting the functioning of the hypothalamic-pituitary-adrenal axis, sympathetic nervous system, cardiovascular system, and metabolic processes, and lymphocyte changes typically affiliated with aging in a cohort of healthy volunteers ranging from 18 to 66 y. RESULTS: Physiological stress load positively correlated with subject age in the study cohort and was significantly higher in adults 50–66 y compared to adults 18–33 y and 34–49 y. Using physiological stress load, we identified a significant age-dependent association between stress load and frequencies of circulating regulatory T lymphocytes (Tregs). Frequencies were higher in younger participants, but only in participants exhibiting low physiological stress load. As stress load increased, frequencies of Tregs decreased in young participants but were unchanged with increasing stress load in middle and older age individuals. Follow-up analysis of stress load components indicated lower circulating DHEA-S and higher urinary norepinephrine as the primary contributors to the effects of total stress load on Tregs. In addition, we identified age-independent inverse associations between stress load and frequencies of naïve Tregs and naïve CD4 T cells and positive associations between stress load and frequencies of memory Tregs and memory CD4 T cells. These associations were primarily driven by stress load components waist circumference, systolic and diastolic blood pressure, CRP, and HbA1c. In summary, our study results suggest that, in younger people, physiological stress load may diminish regulatory T cell frequencies to levels seen in older persons. Furthermore, independent of age, stress load may contribute to contraction of the naïve Treg pool and accumulation of memory Treg cells. CLINICAL TRIAL: Registered on ClincialTrials.gov (Identifier: NCT02367287). SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12979-023-00357-5. BioMed Central 2023-06-23 /pmc/articles/PMC10288764/ /pubmed/37353855 http://dx.doi.org/10.1186/s12979-023-00357-5 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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.
spellingShingle Research
Snodgrass, Ryan G.
Jiang, Xiaowen
Stephensen, Charles B.
Laugero, Kevin D.
Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title_full Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title_fullStr Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title_full_unstemmed Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title_short Cumulative physiological stress is associated with age-related changes to peripheral T lymphocyte subsets in healthy humans
title_sort cumulative physiological stress is associated with age-related changes to peripheral t lymphocyte subsets in healthy humans
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288764/
https://www.ncbi.nlm.nih.gov/pubmed/37353855
http://dx.doi.org/10.1186/s12979-023-00357-5
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