References
-
Lee, K. A., Flores, R. R., Jang, I. H., Saathoff, A. & Robbins, P. D. Immune senescence, immunosenescence and aging. Front. Aging 3, 900028. https://doi.org/10.3389/fragi.2022.900028 (2022).
-
Barbé-Tuana, F., Funchal, G., Schmitz, C. R. R., Maurmann, R. M. & Bauer, M. E. The interplay between immunosenescence and age-related diseases. Semin. Immunopathol. 42, 545–557. https://doi.org/10.1007/s00281-020-00806-z (2020).
-
Santoro, A., Bientinesi, E. & Monti, D. Immunosenescence and inflammaging in the aging process: Age-related diseases or longevity?. Ageing Res. Rev. 71, 101422. https://doi.org/10.1016/j.arr.2021.101422 (2021).
-
Li, X. et al. Inflammation and aging: Signaling pathways and intervention therapies. Signal Transduct. Target. Ther. 8, 239. https://doi.org/10.1038/s41392-023-01502-8 (2023).
-
Ovadya, Y. et al. Impaired immune surveillance accelerates accumulation of senescent cells and aging. Nat. Commun. 9, 5435. https://doi.org/10.1038/s41467-018-07825-3 (2018).
-
Carrasco, E. et al. The role of T cells in age-related diseases. Nat. Rev. Immunol. 22, 97–111. https://doi.org/10.1038/s41577-021-00557-4 (2022).
-
Mittelbrunn, M. & Kroemer, G. Hallmarks of T cell aging. Nat. Immunol. 22, 687–698. https://doi.org/10.1038/s41590-021-00927-z (2021).
-
Tu, W. & Rao, S. Mechanisms underlying T cell immunosenescence: Aging and cytomegalovirus infection. Front. Microbiol. 7, 2111. https://doi.org/10.3389/fmicb.2016.02111 (2016).
-
Weng, N. P., Akbar, A. N. & Goronzy, J. CD28(-) T cells: Their role in the age-associated decline of immune function. Trends Immunol. 30, 306–312. https://doi.org/10.1016/j.it.2009.03.013 (2009).
-
Esensten, J. H., Helou, Y. A., Chopra, G., Weiss, A. & Bluestone, J. A. CD28 costimulation: From mechanism to therapy. Immunity 44, 973–988. https://doi.org/10.1016/j.immuni.2016.04.020 (2016).
-
Boussiotis, V. A., Freeman, G. J., Gribben, J. G. & Nadler, L. M. The critical role of CD28 signalling in the prevention of human T-cell anergy. Res. Immunol. 146, 140–149. https://doi.org/10.1016/0923-2494(96)80247-1 (1995).
-
Mou, D., Espinosa, J., Lo, D. J. & Kirk, A. D. CD28 negative T cells: Is their loss our gain?. Am. J. Transplant. 14, 2460–2466. https://doi.org/10.1111/ajt.12937 (2014).
-
Coleman, M. J., Zimmerly, K. M. & Yang, X. O. Accumulation of CD28(null) senescent T-cells is associated with poorer outcomes in COVID19 patients. Biomolecules https://doi.org/10.3390/biom11101425 (2021).
-
Macaulay, R., Akbar, A. N. & Henson, S. M. The role of the T cell in age-related inflammation. Age 35, 563–572. https://doi.org/10.1007/s11357-012-9381-2 (2013).
-
Pedersen, B. K. & Hoffman-Goetz, L. Exercise and the immune system: Regulation, integration, and adaptation. Physiol. Rev. 80, 1055–1081 (2000).
-
Gleeson, M. et al. The anti-inflammatory effects of exercise: Mechanisms and implications for the prevention and treatment of disease. Nat. Rev. Immunol. 11, 607–615. https://doi.org/10.1038/nri3041 (2011).
-
Wang, J., Liu, S., Li, G. & Xiao, J. Exercise regulates the immune system. Adv. Exp. Med. Biol. 1228, 395–408. https://doi.org/10.1007/978-981-15-1792-1_27 (2020).
-
Wang, Q. & Zhou, W. Roles and molecular mechanisms of physical exercise in cancer prevention and treatment. J. Sport Health Sci. 10, 201–210. https://doi.org/10.1016/j.jshs.2020.07.008 (2021).
-
da Silveira, M. P. et al. Physical exercise as a tool to help the immune system against COVID-19: An integrative review of the current literature. Clin. Exp. Med. 21, 15–28. https://doi.org/10.1007/s10238-020-00650-3 (2021).
-
Donovan, T., Bain, A. L., Tu, W., Pyne, D. B. & Rao, S. Influence of exercise on exhausted and senescent T cells: A systematic review. Front. Physiol. 12, 668327. https://doi.org/10.3389/fphys.2021.668327 (2021).
-
de Carvalho-Costa, T. M. et al. Immunophenotypic analysis of T lymphocytes and cytokine production in elderly practicing physical activities and its relationship with quality of life and depression. Oxid. Med. Cell. Longev. 2022, 7985596. https://doi.org/10.1155/2022/7985596 (2022).
-
Krüger, K., Mooren, F. C. & Pilat, C. The immunomodulatory effects of physical activity. Curr. Pharm. Des. 22, 3730–3748. https://doi.org/10.2174/1381612822666160322145107 (2016).
-
Walzik, D. et al. Impact of exercise on markers of B cell-related immunity: A systematic review. J. Sport Health Sci. https://doi.org/10.1016/j.jshs.2023.10.002 (2023).
-
Theall, B. et al. Impact of acute exercise on peripheral blood mononuclear cells nutrient sensing and mitochondrial oxidative capacity in healthy young adults. Physiol. Rep. 9, e15147. https://doi.org/10.14814/phy2.15147 (2021).
-
de Almeida-Neto, P. F. et al. Influence of age and fitness level on immune responses of T and NK cells in healthy physically active subjects after strenuous aerobic exercise: A cross-sectional study. Front. Immunol. 14, 1252506. https://doi.org/10.3389/fimmu.2023.1252506 (2023).
-
Campbell, J. P. et al. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effector-memory phenotype. Brain Behav. Immunol. 23, 767–775. https://doi.org/10.1016/j.bbi.2009.02.011 (2009).
-
Siedlik, J. A. et al. T cell activation and proliferation following acute exercise in human subjects is altered by storage conditions and mitogen selection. J. Immunol. Methods 446, 7–14. https://doi.org/10.1016/j.jim.2017.03.017 (2017).
-
Mazur, M. et al. Effects of controlled physical activity on immune cell phenotype in peripheral blood in prehypertension—Studies in preclinical model and randomised crossover study. J. Physiol. Pharmacol. https://doi.org/10.26402/jpp.2018.6.12 (2018).
-
Woods, J. A. et al. Effects of 6 months of moderate aerobic exercise training on immune function in the elderly. Mech. Ageing Dev. 109, 1–19. https://doi.org/10.1016/S0047-6374(99)00014-7 (1999).
-
Lowder, T., Padgett, D. A. & Woods, J. A. Moderate exercise protects mice from death due to influenza virus. Brain Behav. Immun. 19, 377–380. https://doi.org/10.1016/j.bbi.2005.04.002 (2005).
-
Jones, H. H., Priest, J. D., Hayes, W. C., Tichenor, C. C. & Nagel, D. A. Humeral hypertrophy in response to exercise. J. Bone Joint Surg. 59, 204–208 (1977).
-
Blanks, A. M. et al. Whole body vibration elicits differential immune and metabolic responses in obese and normal weight individuals. Brain Behav Immun Health 1, 100011. https://doi.org/10.1016/j.bbih.2019.100011 (2020).
-
Pagnotti, G. M. et al. Combating osteoporosis and obesity with exercise: Leveraging cell mechanosensitivity. Nat. Rev. Endocrinol. 15, 339–355. https://doi.org/10.1038/s41574-019-0170-1 (2019).
-
Rubin, C. T. et al. Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc. Natl. Acad. Sci. U. S. A. 104, 17879–17884. https://doi.org/10.1073/pnas.0708467104 (2007).
-
Di, X. et al. Cellular mechanotransduction in health and diseases: From molecular mechanism to therapeutic targets. Signal Transduct. Target. Ther. 8, 282. https://doi.org/10.1038/s41392-023-01501-9 (2023).
-
Yano, S., Komine, M., Fujimoto, M., Okochi, H. & Tamaki, K. Activation of Akt by mechanical stretching in human epidermal keratinocytes. Exp. Dermatol. 15, 356–361. https://doi.org/10.1111/j.0906-6705.2006.00425.x (2006).
-
Fritton, S. P., McLeod, K. J. & Rubin, C. T. Quantifying the strain history of bone: Spatial uniformity and self-similarity of low-magnitude strains. J. Biomech. 33, 317–325 (2000).
-
Ozcivici, E. et al. Mechanical signals as anabolic agents in bone. Nat. Rev. Rheumatol. 6, 50–59 (2010).
-
Uzer, G., Pongkitwitoon, S., Ete Chan, M. & Judex, S. Vibration induced osteogenic commitment of mesenchymal stem cells is enhanced by cytoskeletal remodeling but not fluid shear. J. Biomech. 46, 2296–2302. https://doi.org/10.1016/j.jbiomech.2013.06.008 (2013).
-
Uzer, G. et al. Separating fluid shear stress from acceleration during vibrations in vitro: Identification of mechanical signals modulating the cellular response. Cell. Mol. Bioeng. 5, 266–276 (2012).
-
Mousset, C. M. et al. Comprehensive phenotyping of T cells using flow cytometry. Cytometry A 95, 647–654. https://doi.org/10.1002/cyto.a.23724 (2019).
-
Wherry, E. J. & Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15, 486–499. https://doi.org/10.1038/nri3862 (2015).
-
Xie, L., Rubin, C. & Judex, S. Enhancement of the adolescent murine musculoskeletal system using low-level mechanical vibrations. J. Appl. Physiol. 104, 1056–1062 (2008).
-
Patel, V. S. et al. Incorporating refractory period in mechanical stimulation mitigates obesity-induced adipose tissue dysfunction in adult mice. Obesity https://doi.org/10.1002/oby.21958 (2017).
-
Sen, B. et al. Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. J. Biomech. 44, 593–599. https://doi.org/10.1016/j.jbiomech.2010.11.022 (2011).
-
Fry, R. W., Morton, A. R., Crawford, G. P. & Keast, D. Cell numbers and in vitro responses of leucocytes and lymphocyte subpopulations following maximal exercise and interval training sessions of different intensities. Eur. J. Appl. Physiol. Occup. Physiol. 64, 218–227. https://doi.org/10.1007/bf00626284 (1992).
-
De Belly, H., Paluch, E. K. & Chalut, K. J. Interplay between mechanics and signalling in regulating cell fate. Nat. Rev. Mol. Cell Biol. 23, 465–480. https://doi.org/10.1038/s41580-022-00472-z (2022).
-
Green, K. J., Rowbottom, D. G. & Mackinnon, L. T. Acute exercise and T-lymphocyte expression of the early activation marker CD69. Med. Sci. Sports Exerc. 35, 582–588. https://doi.org/10.1249/01.Mss.0000058361.82096.26 (2003).
-
Uzeloto, J. S. et al. Effect of physical training on cytokine expression in CD4+ T lymphocytes in subjects with stable COPD. Ther. Adv. Respir. Dis. 16, 17534666221091180. https://doi.org/10.1177/17534666221091179 (2022).
-
Shaw, D. M., Merien, F., Braakhuis, A. & Dulson, D. T-cells and their cytokine production: The anti-inflammatory and immunosuppressive effects of strenuous exercise. Cytokine 104, 136–142. https://doi.org/10.1016/j.cyto.2017.10.001 (2018).
-
Mooren, F. C., Lechtermann, A., Fromme, A., Thorwesten, L. & Völker, K. Alterations in intracellular calcium signaling of lymphocytes after exhaustive exercise. Med. Sci. Sports Exerc. 33, 242–248. https://doi.org/10.1097/00005768-200102000-00012 (2001).
-
Kane, L. P., Andres, P. G., Howland, K. C., Abbas, A. K. & Weiss, A. Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-gamma but not TH2 cytokines. Nat. Immunol. 2, 37–44. https://doi.org/10.1038/83144 (2001).
-
Yi, J. S., Cox, M. A. & Zajac, A. J. T-cell exhaustion: Characteristics, causes and conversion. Immunology 129, 474–481. https://doi.org/10.1111/j.1365-2567.2010.03255.x (2010).
-
Blank, C. U. et al. Defining ‘T cell exhaustion’. Nat. Rev. Immunol. 19, 665–674. https://doi.org/10.1038/s41577-019-0221-9 (2019).
-
Kasakovski, D., Xu, L. & Li, Y. T cell senescence and CAR-T cell exhaustion in hematological malignancies. J. Hematol. Oncol. 11, 91. https://doi.org/10.1186/s13045-018-0629-x (2018).
-
Zhang, Z. et al. T cell dysfunction and exhaustion in cancer. Front. Cell Dev. Biol. 8, 17. https://doi.org/10.3389/fcell.2020.00017 (2020).
-
Dolina, J. S., Van Braeckel-Budimir, N., Thomas, G. D. & Salek-Ardakani, S. CD8(+) T cell exhaustion in cancer. Front. Immunol. 12, 715234. https://doi.org/10.3389/fimmu.2021.715234 (2021).
-
Krueger, J., Rudd, C. E. & Taylor, A. Seminars in Immunology. 101295 (Elsevier).
-
Taylor, A. et al. Glycogen synthase kinase 3 inactivation drives T-bet-mediated downregulation of co-receptor PD-1 to enhance CD8+ cytolytic T cell responses. Immunity 44, 274–286 (2016).
-
Rudd, C. E., Chanthong, K. & Taylor, A. Small molecule inhibition of GSK-3 specifically inhibits the transcription of inhibitory co-receptor LAG-3 for enhanced anti-tumor immunity. Cell Rep. 30, 2075-2082. e2074 (2020).
-
Taylor, A., Rothstein, D. & Rudd, C. E. Small-molecule inhibition of PD-1 transcription is an effective alternative to antibody blockade in cancer therapy. Cancer Res. 78, 706–717 (2018).
-
Velden, JLJvd. et al. Myogenic differentiation during regrowth of atrophied skeletal muscle is associated with inactivation of GSK-3β. Am. J. Physiol.-Cell Physiol. 292, C1636–C1644. https://doi.org/10.1152/ajpcell.00504.2006 (2007).
-
Sen, B. et al. Mechanically induced focal adhesion assembly amplifies anti-adipogenic pathways in mesenchymal stem cells. Stem Cells 29, 1829–1836. https://doi.org/10.1002/stem.732 (2011).
-
Newberg, J. et al. Isolated nuclei stiffen in response to low intensity vibration. J. Biomech. 111, 110012 (2020).
-
Appleman, L. J., van Puijenbroek, A. A., Shu, K. M., Nadler, L. M. & Boussiotis, V. A. CD28 costimulation mediates down-regulation of p27kip1 and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J. Immunol. 168, 2729–2736. https://doi.org/10.4049/jimmunol.168.6.2729 (2002).
-
Bhavsar, S. K., Merches, K., Bobbala, D. & Lang, F. AKT/SGK-sensitive phosphorylation of GSK3 in the regulation of L-selectin and perforin expression as well as activation induced cell death of T-lymphocytes. Biochem. Biophys. Res. Commun. 425, 6–12. https://doi.org/10.1016/j.bbrc.2012.07.030 (2012).
-
Zhu, C., Chen, W., Lou, J., Rittase, W. & Li, K. Mechanosensing through immunoreceptors. Nat. Immunol. 20, 1269–1278. https://doi.org/10.1038/s41590-019-0491-1 (2019).
-
Wang, J. H. T cell receptors, mechanosensors, catch bonds and immunotherapy. Prog. Biophys. Mol. Biol. 153, 23–27. https://doi.org/10.1016/j.pbiomolbio.2020.01.001 (2020).
-
Liu, B., Kolawole, E. M. & Evavold, B. D. Mechanobiology of T cell activation: To catch a bond. Annu. Rev. Cell Dev. Biol. 37, 65–87. https://doi.org/10.1146/annurev-cellbio-120219-055100 (2021).
-
Chan, M. E. et al. Low intensity mechanical signals promote proliferation in a cell-specific manner: Tailoring a non-drug strategy to enhance biomanufacturing yields. bioRxiv https://doi.org/10.1101/2023.07.05.547864 (2023).
-
Trickett, A. & Kwan, Y. L. T cell stimulation and expansion using anti-CD3/CD28 beads. J. Immunol. Methods 275, 251–255. https://doi.org/10.1016/s0022-1759(03)00010-3 (2003).
-
Fearon, D. T. The expansion and maintenance of antigen-selected CD8(+) T cell clones. Adv. Immunol. 96, 103–139. https://doi.org/10.1016/s0065-2776(07)96003-4 (2007).
