Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial

Abstract Background Immunosenescence is described as age-associated changes within the immune system that are responsible for decreased immunity and increased cancer risk. Physically active individuals have fewer ‘senescent’ and more naïve T-cells compared to their sedentary counterparts, but it is...

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Main Authors: Grace M Niemiro, Adriana M Coletta, Nadia H. Agha, Preteesh Leo Mylabathula, Forrest L. Baker, Abenaa M Brewster, Therese B Bevers, Enrique Fuentes-Mattei, Karen Basen-Engquist, Emmanuel Katsanis, Susan C Gilchrist, Richard J. Simpson
Format: Article
Language:English
Published: BMC 2022-03-01
Series:Immunity & Ageing
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Online Access:https://doi.org/10.1186/s12979-022-00266-z
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author Grace M Niemiro
Adriana M Coletta
Nadia H. Agha
Preteesh Leo Mylabathula
Forrest L. Baker
Abenaa M Brewster
Therese B Bevers
Enrique Fuentes-Mattei
Karen Basen-Engquist
Emmanuel Katsanis
Susan C Gilchrist
Richard J. Simpson
author_facet Grace M Niemiro
Adriana M Coletta
Nadia H. Agha
Preteesh Leo Mylabathula
Forrest L. Baker
Abenaa M Brewster
Therese B Bevers
Enrique Fuentes-Mattei
Karen Basen-Engquist
Emmanuel Katsanis
Susan C Gilchrist
Richard J. Simpson
author_sort Grace M Niemiro
collection DOAJ
description Abstract Background Immunosenescence is described as age-associated changes within the immune system that are responsible for decreased immunity and increased cancer risk. Physically active individuals have fewer ‘senescent’ and more naïve T-cells compared to their sedentary counterparts, but it is not known if exercise training can rejuvenate ‘older looking’ T-cell profiles. We determined the effects of 12-weeks supervised exercise training on the frequency of T-cell subtypes in peripheral blood and their relationships with circulating levels of the muscle-derived cytokines (i.e. ‘myokines’) IL-6, IL-7, IL-15 and osteonectin in older women at high risk of breast cancer. The intervention involved 3 sessions/week of either high intensity interval exercise (HIIT) or moderate intensity continuous exercise (MICT) and were compared to an untrained control (UC) group. Results HIIT decreased total granulocytes, CD4+ T-cells, CD4+ naïve T-cells, CD4+ recent thymic emigrants (RTE) and the CD4:CD8 ratio after training, whereas MICT increased total lymphocytes and CD8 effector memory (EM) T-cells. The change in total T-cells, CD4+ naïve T-cells, CD4+ central memory (CM) T-cells and CD4+ RTE was elevated after MICT compared to HIIT. Changes in V ̇ O 2 max $$ \dot{\mathrm{V}}{\mathrm{O}}_{2\max } $$ after training, regardless of exercise prescription, was inversely related to the change in highly differentiated CD8+ EMRA T-cells and positively related to changes in β2-adrenergic receptor (β2-AR) expression on CM CD4+ and CM CD8+ T-cells. Plasma myokine levels did not change significantly among the groups after training, but individual changes in IL-7 were positively related to changes in the number of β2-AR expressing CD4 naïve T cells in both exercise groups but not controls. Further, CD4 T-cells and CD4 naive T-cells were negatively related to changes in IL-6 and osteonectin after HIIT but not MICT, whereas CD8 EMRA T-cells were inversely related to changes in IL-15 after MICT but not HIIT. Conclusions Aerobic exercise training alters the frequency of peripheral T-cells associated with immunosenescence in middle aged/older women at high risk of breast cancer, with HIIT (pro-senescent) and MICT (anti-senescent) evoking divergent effects. Identifying the underlying mechanisms and establishing whether exercise-induced changes in peripheral T-cell numbers can alter the risk of developing breast cancer warrants investigation.
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spelling doaj.art-daa70918ea9c414d873c4b1e49fb023f2022-12-21T23:32:38ZengBMCImmunity & Ageing1742-49332022-03-0119111510.1186/s12979-022-00266-zSalutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trialGrace M Niemiro0Adriana M Coletta1Nadia H. Agha2Preteesh Leo Mylabathula3Forrest L. Baker4Abenaa M Brewster5Therese B Bevers6Enrique Fuentes-Mattei7Karen Basen-Engquist8Emmanuel Katsanis9Susan C Gilchrist10Richard J. Simpson11Department of Pediatrics, The University of ArizonaDepartment of Health and Kinesiology, The University of UtahDepartment of Health and Human Performance, University of HoustonDepartment of Pediatrics, The University of ArizonaDepartment of Pediatrics, The University of ArizonaDepartment of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer CenterDepartment of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer CenterDepartment of Radiation Oncology Clinical Research, The University of Texas MD Anderson Cancer CenterDepartment of Behavioral Science, The University of Texas MD Anderson Cancer CenterDepartment of Pediatrics, The University of ArizonaDepartment of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer CenterDepartment of Pediatrics, The University of ArizonaAbstract Background Immunosenescence is described as age-associated changes within the immune system that are responsible for decreased immunity and increased cancer risk. Physically active individuals have fewer ‘senescent’ and more naïve T-cells compared to their sedentary counterparts, but it is not known if exercise training can rejuvenate ‘older looking’ T-cell profiles. We determined the effects of 12-weeks supervised exercise training on the frequency of T-cell subtypes in peripheral blood and their relationships with circulating levels of the muscle-derived cytokines (i.e. ‘myokines’) IL-6, IL-7, IL-15 and osteonectin in older women at high risk of breast cancer. The intervention involved 3 sessions/week of either high intensity interval exercise (HIIT) or moderate intensity continuous exercise (MICT) and were compared to an untrained control (UC) group. Results HIIT decreased total granulocytes, CD4+ T-cells, CD4+ naïve T-cells, CD4+ recent thymic emigrants (RTE) and the CD4:CD8 ratio after training, whereas MICT increased total lymphocytes and CD8 effector memory (EM) T-cells. The change in total T-cells, CD4+ naïve T-cells, CD4+ central memory (CM) T-cells and CD4+ RTE was elevated after MICT compared to HIIT. Changes in V ̇ O 2 max $$ \dot{\mathrm{V}}{\mathrm{O}}_{2\max } $$ after training, regardless of exercise prescription, was inversely related to the change in highly differentiated CD8+ EMRA T-cells and positively related to changes in β2-adrenergic receptor (β2-AR) expression on CM CD4+ and CM CD8+ T-cells. Plasma myokine levels did not change significantly among the groups after training, but individual changes in IL-7 were positively related to changes in the number of β2-AR expressing CD4 naïve T cells in both exercise groups but not controls. Further, CD4 T-cells and CD4 naive T-cells were negatively related to changes in IL-6 and osteonectin after HIIT but not MICT, whereas CD8 EMRA T-cells were inversely related to changes in IL-15 after MICT but not HIIT. Conclusions Aerobic exercise training alters the frequency of peripheral T-cells associated with immunosenescence in middle aged/older women at high risk of breast cancer, with HIIT (pro-senescent) and MICT (anti-senescent) evoking divergent effects. Identifying the underlying mechanisms and establishing whether exercise-induced changes in peripheral T-cell numbers can alter the risk of developing breast cancer warrants investigation.https://doi.org/10.1186/s12979-022-00266-zPhysical activityMyokinesExercise immunologyβ2 adrenergic receptorAgingMaximal oxygen uptake
spellingShingle Grace M Niemiro
Adriana M Coletta
Nadia H. Agha
Preteesh Leo Mylabathula
Forrest L. Baker
Abenaa M Brewster
Therese B Bevers
Enrique Fuentes-Mattei
Karen Basen-Engquist
Emmanuel Katsanis
Susan C Gilchrist
Richard J. Simpson
Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
Immunity & Ageing
Physical activity
Myokines
Exercise immunology
β2 adrenergic receptor
Aging
Maximal oxygen uptake
title Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
title_full Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
title_fullStr Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
title_full_unstemmed Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
title_short Salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral T-cells associated with immunosenescence in older women at high risk of breast cancer: a randomized controlled trial
title_sort salutary effects of moderate but not high intensity aerobic exercise training on the frequency of peripheral t cells associated with immunosenescence in older women at high risk of breast cancer a randomized controlled trial
topic Physical activity
Myokines
Exercise immunology
β2 adrenergic receptor
Aging
Maximal oxygen uptake
url https://doi.org/10.1186/s12979-022-00266-z
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