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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

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Mini-Review Article

New Insights about Regulatory T Cells Distribution and Function with Exercise: The Role of Immunometabolism

Author(s): Gilson P. Dorneles*, Aline A.Z. dos Passos, Pedro R.T. Romão and Alessandra Peres*

Volume 26, Issue 9, 2020

Page: [979 - 990] Pages: 12

DOI: 10.2174/1381612826666200305125210

Price: $65

Abstract

A lack of physical activity is linked to the development of many chronic diseases through a chronic low-grade inflammation state. It is now well accepted that the immune system plays a central role in the development of several chronic diseases, including insulin resistance, type 2 diabetes, atherosclerosis, heart failure and certain types of cancer. Exercise elicits a strong anti-inflammatory response independently of weight loss and can be a useful non-pharmacologic strategy to counteract the low-grade inflammation. The CD4+CD25+CD127- FoxP3+ Regulatory T (Treg) cells are a unique subset of helper T-cells, which regulate immune response and establish self-tolerance through the secretion of immunoregulatory cytokines, such as IL-10 and TGF-β, and the suppression of the function and activity of many immune effector cells (including monocytes/macrophages, dendritic cells, CD4+ and CD8+ T cells, and Natural Killers). The metabolic phenotype of Tregs are regulated by the transcription factor Foxp3, providing flexibility in fuel choice, but a preference for higher fatty acid oxidation. In this review, we focus on the mechanisms by which exercise - both acute and chronic - exerts its antiinflammatory effects through Treg cells mobilization. Furthermore, we discuss the implications of immunometabolic changes during exercise for the modulation of Treg phenotype and its immunosuppressive function. This narrative review focuses on the current knowledge regarding the role of Treg cells in the context of acute and chronic exercise using data from observational and experimental studies. Emerging evidence suggests that the immunomodulatory effects of exercise are mediated by the ability of exercise to adjust and improve Tregs number and function.

Keywords: Treg cells, FoxP3, immunometabolism, cardiorrespiratory fitness, physical activity, exercise, inflammation.

« Previous
[1]
Booth FW, Roberts CK, Thyfault JP, Ruegsegger GN, Toedebusch RG. Role of inactivity in chronic diseases: evolutionary insight and pathophysiological mechanisms. Physiol Rev 2017; 97(4): 1351-402.
[2]
Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 2011; 11(9): 607-15.
[http://dx.doi.org/10.1038/nri3041] [PMID: 21818123]
[3]
Walsh NP, Gleeson M, Shephard RJ, et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63.
[4]
Simpson RJ, Kunz H, Agha N, Graff R. Exercise and the regulation of immune functions. 1st ed. Progress in Molecular Biology and Translational Science. Elsevier Inc. 2015; p. 355-80.
[5]
Newton R, Priyadharshini B, Turka LA. Immunometabolism of regulatory T cells. Nat Immunol 2016; 17(6): 618-25.
[http://dx.doi.org/10.1038/ni.3466] [PMID: 27196520]
[6]
You T, Arsenis NC, Disanzo BL, Lamonte MJ. Effects of exercise training on chronic inflammation in obesity : current evidence and potential mechanisms. Sports Med 2013; 43(4): 243-56.
[http://dx.doi.org/10.1007/s40279-013-0023-3] [PMID: 23494259]
[7]
Vignali DAA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8(7): 523-32.
[http://dx.doi.org/10.1038/nri2343] [PMID: 18566595]
[8]
Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010; 11(1): 7-13.
[http://dx.doi.org/10.1038/ni.1818] [PMID: 20016504]
[9]
Walsh NP, Gleeson M, Shephard RJ, et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63.
[PMID: 21446352]
[10]
Nimmo MA, Leggate M, Viana JL, King JA. The effect of physical activity on mediators of inflammation. Diabetes Obes Metab 2013; 15(Suppl. 3): 51-60.
[http://dx.doi.org/10.1111/dom.12156] [PMID: 24003921]
[11]
Turner JE, Wadley AJ, Aldred S, Fisher JP, Bosch JA, Campbell JP. Intensive exercise does not preferentially mobilize skin-homing t cells and NK cells. Med Sci Sports Exerc 2016; 48(7): 1285-93.
[http://dx.doi.org/10.1249/MSS.0000000000000914] [PMID: 26918560]
[12]
Malm C. Exercise immunology: the current state of man and mouse. Sports Med 2004; 34(9): 555-66.
[http://dx.doi.org/10.2165/00007256-200434090-00001] [PMID: 15294006]
[13]
Krüger K, Mooren FC, Pilat C. The immunomodulatory effects of physical activity. Curr Pharm Des 2016; 22(24): 3730-48.
[http://dx.doi.org/10.2174/1381612822666160322145107] [PMID: 27000826]
[14]
Rooney BV, Bigley AB, LaVoy EC, Laughlin M, Pedlar C, Simpson RJ. Lymphocytes and monocytes egress peripheral blood within minutes after cessation of steady state exercise: A detailed temporal analysis of leukocyte extravasation. Physiol Behav 2018; 194: 260-7.
[http://dx.doi.org/10.1016/j.physbeh.2018.06.008] [PMID: 29885920]
[15]
Krüger K, Lechtermann A, Fobker M, Völker K, Mooren FC. Exercise-induced redistribution of T lymphocytes is regulated by adrenergic mechanisms. Brain Behav Immun 2008; 22(3): 324-38.
[http://dx.doi.org/10.1016/j.bbi.2007.08.008] [PMID: 17910910]
[16]
Campbell JP, Turner JE. Debunking the myth of exercise-induced immune suppression: redefining the impact of exercise on immunological health across the lifespan. Front Immunol 2018; 9: 648.
[http://dx.doi.org/10.3389/fimmu.2018.00648] [PMID: 29713319]
[17]
Kostrzewa-Nowak D, Nowak R. Analysis of selected T cell subsets in peripheral blood after exhaustive effort among elite soccer players. Biochem Med (Zagreb) 2018; 28(3)030707
[http://dx.doi.org/10.11613/BM.2018.030707] [PMID: 30429675]
[18]
Curran M, Campbell J, Drayson M, Andrews R, Narendran P. Type 1 diabetes impairs the mobilisation of highly-differentiated CD8+T cells during a single bout of acute exercise. Exerc Immunol Rev 2019; 25: 64-82.
[PMID: 30753130]
[19]
Deuster PA, Curiale AM, Cowan ML, Finkelman FD. Exercise-induced changes in populations of peripheral blood mononuclear cells. Med Sci Sports Exerc 1988; 20(3): 276-80.
[http://dx.doi.org/10.1249/00005768-198806000-00011] [PMID: 3260323]
[20]
Cosgrove C, Galloway SDR, Neal C, et al. The impact of 6-month training preparation for an Ironman triathlon on the proportions of naïve, memory and senescent T cells in resting blood. Eur J Appl Physiol 2012; 112(8): 2989-98.
[http://dx.doi.org/10.1007/s00421-011-2273-9] [PMID: 22170013]
[21]
Dorneles GP, Boeira MCR, Schipper LL, et al. Acute strenuous exercise induces an imbalance on histone H4 acetylation/histone deacetylase 2 and increases the proinflammatory profile of PBMC of obese individuals. Oxid Med Cell Longev 2017; 2017.
[22]
Timmons BW, Tarnopolsky MA, Snider DP, Bar-Or O. Puberty effects on NK cell responses to exercise and carbohydrate intake in boys. Med Sci Sports Exerc 2006; 38(5): 864-74.
[http://dx.doi.org/10.1249/01.mss.0000218124.87917.40] [PMID: 16672839]
[23]
Campbell JP, Riddell NE, Burns VE, et al. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effector-memory phenotype. Brain Behav Immun 2009; 23(6): 767-75.
[http://dx.doi.org/10.1016/j.bbi.2009.02.011] [PMID: 19254756]
[24]
Simpson RJ, Cosgrove C, Chee MM, et al. Senescent phenotypes and telomere lengths of peripheral blood T-cells mobilized by acute exercise in humans. Exerc Immunol Rev 2010; 16: 40-55.
[PMID: 20839490]
[25]
Wonner R, Wallner S, Orsó E, Schmitz G. Effects of acute exercise on monocyte subpopulations in metabolic syndrome patients. Cytom Part B - Clin Cytom 2018; 94(4): 596-605.
[http://dx.doi.org/10.1002/cyto.b.21387]
[26]
Peres A, Lima DDD, Dorneles GP, et al. Expression of CCr5 on immune cells after eccentric or concentric isokinetic exercise. Isokinet Exerc Sci 2017; 25(1)
[http://dx.doi.org/10.3233/IES-160647]
[27]
Graff RM, Kunz HE, Agha NH, et al. β2-Adrenergic receptor signaling mediates the preferential mobilization of differentiated subsets of CD8+ T-cells, NK-cells and non-classical monocytes in response to acute exercise in humans. Brain Behav Immun 2018; 74: 143-53.
[http://dx.doi.org/10.1016/j.bbi.2018.08.017] [PMID: 30172948]
[28]
Pacella I, Piconese S. Immunometabolic checkpoints of treg dynamics: adaptation to microenvironmental opportunities and challenges. Front Immunol 2019; 10: 1889.
[http://dx.doi.org/10.3389/fimmu.2019.01889] [PMID: 31507585]
[29]
Liu W, Putnam AL, Xu-Yu Z, et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 2006; 203(7): 1701-11.
[http://dx.doi.org/10.1084/jem.20060772] [PMID: 16818678]
[30]
Sakaguchi S, Ono M, Setoguchi R, et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212: 8-27.
[http://dx.doi.org/10.1111/j.0105-2896.2006.00427.x] [PMID: 16903903]
[31]
Curotto de Lafaille MA, Lafaille JJ. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 2009; 30(5): 626-35.
[http://dx.doi.org/10.1016/j.immuni.2009.05.002] [PMID: 19464985]
[32]
Goldstein JD, Pérol L, Zaragoza B, Baeyens A, Marodon G, Piaggio E. Role of cytokines in thymus- versus peripherally derived-regulatory T cell differentiation and function. Front Immunol 2013; 4: 155.
[http://dx.doi.org/10.3389/fimmu.2013.00155] [PMID: 23801992]
[33]
Kang J, Huddleston SJ, Fraser JM, Khoruts A. De novo induction of antigen-specific CD4+CD25+Foxp3+ regulatory T cells in vivo following systemic antigen administration accompanied by blockade of mTOR. J Leukoc Biol 2008; 83(5): 1230-9.
[http://dx.doi.org/10.1189/jlb.1207851] [PMID: 18270248]
[34]
Liu M, Li S, Li MO. TGF-β control of adaptive immune tolerance: a break from treg cells. BioEssays 2018; 40(11)e1800063
[http://dx.doi.org/10.1002/bies.201800063] [PMID: 30159904]
[35]
Sanjabi S, Oh SA, Li MO. Regulation of the immune response by TGF-β: from conception to autoimmunity and infection. Cold Spring Harb Perspect Biol 2017; 9(6)a022236
[http://dx.doi.org/10.1101/cshperspect.a022236] [PMID: 28108486]
[36]
Schottelius AJG, Mayo MW, Sartor RB, Baldwin AS Jr. Interleukin-10 signaling blocks inhibitor of kappaB kinase activity and nuclear factor kappaB DNA binding. J Biol Chem 1999; 274(45): 31868-74.
[http://dx.doi.org/10.1074/jbc.274.45.31868] [PMID: 10542212]
[37]
Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6(11): 1133-41.
[http://dx.doi.org/10.1038/ni1261] [PMID: 16200068]
[38]
Brunet JF, Denizot F, Luciani MF, et al. A new member of the immunoglobulin superfamily--CTLA-4. Nature 1987; 328(6127): 267-70.
[39]
Lindsten T, Lee KP, Harris ES, et al. Characterization of CTLA-4 structure and expression on human T cells. J Immunol 1993; 151(7): 3489-99.
[PMID: 8397258]
[40]
Bono MR, Fernández D, Flores-Santibáñez F, Rosemblatt M, Sauma D. CD73 and CD39 ectonucleotidases in T cell differentiation: Beyond immunosuppression. FEBS Lett 2015; 589(22): 3454-60.
[http://dx.doi.org/10.1016/j.febslet.2015.07.027] [PMID: 26226423]
[41]
Deaglio S, Dwyer KM, Gao W, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204(6): 1257-65.
[http://dx.doi.org/10.1084/jem.20062512] [PMID: 17502665]
[42]
Antonioli L, Pacher P, Vizi ES, Haskó G. CD39 and CD73 in immunity and inflammation. Trends Mol Med 2013; 19(6): 355-67.
[http://dx.doi.org/10.1016/j.molmed.2013.03.005] [PMID: 23601906]
[43]
Ohta A, Kini R, Ohta A, Subramanian M, Madasu M, Sitkovsky M. The development and immunosuppressive functions of CD4(+) CD25(+) FoxP3(+) regulatory T cells are under influence of the adenosine-A2A adenosine receptor pathway. Front Immunol 2012; 3: 190.
[http://dx.doi.org/10.3389/fimmu.2012.00190] [PMID: 22783261]
[44]
Fletcher JM, Lonergan R, Costelloe L, et al. CD39+Foxp3+ regulatory T Cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol 2009; 183(11): 7602-10.
[http://dx.doi.org/10.4049/jimmunol.0901881] [PMID: 19917691]
[45]
Yegutkin GG. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 2008; 1783(5): 673-94.
[http://dx.doi.org/10.1016/j.bbamcr.2008.01.024] [PMID: 18302942]
[46]
Cluxton D, Petrasca A, Moran B, Fletcher JM. Differential regulation of human treg and Th17 cells by fatty acid synthesis and glycolysis. Front Immunol 2019; 10: 115.
[http://dx.doi.org/10.3389/fimmu.2019.00115] [PMID: 30778354]
[47]
Michalek RD, Gerriets VA, Jacobs SR, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol 2011; 186(6): 3299-303.
[http://dx.doi.org/10.4049/jimmunol.1003613] [PMID: 21317389]
[48]
Angelin A, Gil-de-Gómez L, Dahiya S, et al. Foxp3 reprograms t cell metabolism to function in low-glucose, high-lactate environments. Cell Metab 2017; 25(6): 1282-93.
[49]
Hoeppli RE, Wu D, Cook L, Levings MK. The environment of regulatory T cell biology: cytokines, metabolites, and the microbiome. Front Immunol 2015; 6: 61.
[http://dx.doi.org/10.3389/fimmu.2015.00061] [PMID: 25741338]
[50]
Westendorf AM, Skibbe K, Adamczyk A, et al. Hypoxia enhances immunosuppression by inhibiting CD4+ Effector T cell function and promoting treg activity. Cell Physiol Biochem 2017; 41(4): 1271-84.
[http://dx.doi.org/10.1159/000464429] [PMID: 28278498]
[51]
Gerriets VA, Kishton RJ, Nichols AG, et al. Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J Clin Invest 2015; 125(1): 194-207.
[http://dx.doi.org/10.1172/JCI76012] [PMID: 25437876]
[52]
Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 2010; 33(3): 301-11.
[http://dx.doi.org/10.1016/j.immuni.2010.09.002] [PMID: 20870173]
[53]
Han JM, Patterson SJ, Speck M, Ehses JA, Levings MK. Insulin inhibits IL-10-mediated regulatory T cell function: implications for obesity. J Immunol 2014; 192(2): 623-9.
[http://dx.doi.org/10.4049/jimmunol.1302181] [PMID: 24323581]
[54]
Higashiyama M, Hokari R, Hozumi H, et al. HIF-1 in T cells ameliorated dextran sodium sulfate-induced murine colitis. J Leukoc Biol 2012; 91(6): 901-9.
[http://dx.doi.org/10.1189/jlb.1011518] [PMID: 22457366]
[55]
Sun Y, Tian T, Gao J, et al. Metformin ameliorates the development of experimental autoimmune encephalomyelitis by regulating T helper 17 and regulatory T cells in mice. J Neuroimmunol 2016; 292: 58-67.
[http://dx.doi.org/10.1016/j.jneuroim.2016.01.014] [PMID: 26943960]
[56]
Wirthgen E, Hoeflich A, Rebl A, Günther J. Kynurenic acid: the janus-faced role of an immunomodulatory tryptophan metabolite and its link to pathological conditions. Front Immunol 2018; 8: 1957.
[http://dx.doi.org/10.3389/fimmu.2017.01957] [PMID: 29379504]
[57]
Matarese G, Procaccini C, De Rosa V, Horvath TL, La Cava A. Regulatory T cells in obesity: the leptin connection. Trends Mol Med 2010; 16(6): 247-56.
[http://dx.doi.org/10.1016/j.molmed.2010.04.002] [PMID: 20493774]
[58]
Saucillo DC, Gerriets VA, Sheng J, Rathmell JC, Maciver NJ. Leptin metabolically licenses T cells for activation to link nutrition and immunity. J Immunol 2014; 192(1): 136-44.
[http://dx.doi.org/10.4049/jimmunol.1301158] [PMID: 24273001]
[59]
Han JM, Wu D, Denroche HC, Yao Y, Verchere CB, Levings MK. IL-33 Reverses an obesity-induced deficit in visceral adipose tissue ST2+ t regulatory cells and ameliorates adipose tissue inflammation and insulin resistance. J Immunol 2015; 194(10): 4777-83.
[http://dx.doi.org/10.4049/jimmunol.1500020] [PMID: 25870243]
[60]
Chen X, Oppenheim JJ, Winkler-Pickett RT, Ortaldo JR, Howard OMZ. Glucocorticoid amplifies IL-2-dependent expansion of functional FoxP3(+)CD4(+)CD25(+) T regulatory cells in vivo and enhances their capacity to suppress EAE. Eur J Immunol 2006; 36(8): 2139-49.
[http://dx.doi.org/10.1002/eji.200635873] [PMID: 16841298]
[61]
Bhowmick S, Singh A, Flavell RA, Clark RB, O’Rourke J, Cone RE. The sympathetic nervous system modulates CD4(+)FoxP3(+) regulatory T cells via a TGF-β-dependent mechanism. J Leukoc Biol 2009; 86(6): 1275-83.
[http://dx.doi.org/10.1189/jlb.0209107] [PMID: 19741161]
[62]
Xiang L, Marshall GD Jr. Immunomodulatory effects of in vitro stress hormones on FoxP3, Th1/Th2 cytokine and costimulatory molecule mRNA expression in human peripheral blood mononuclear cells. Neuroimmunomodulation 2011; 18(1): 1-10.
[http://dx.doi.org/10.1159/000311450] [PMID: 20606488]
[63]
Nandakumar S, Miller CWT, Kumaraguru U. T regulatory cells: an overview and intervention techniques to modulate allergy outcome. Clin Mol Allergy 2009; 7: 5.
[http://dx.doi.org/10.1186/1476-7961-7-5] [PMID: 19284628]
[64]
Wilson LD, Zaldivar FP, Schwindt CD, Wang-Rodriguez J, Cooper DM. Circulating T-regulatory cells, exercise and the elite adolescent swimmer. Pediatr Exerc Sci 2009; 21(3): 305-17.
[http://dx.doi.org/10.1123/pes.21.3.305] [PMID: 19827454]
[65]
Handzlik MK, Shaw AJ, Dungey M, Bishop NC, Gleeson M. The influence of exercise training status on antigen-stimulated IL-10 production in whole blood culture and numbers of circulating regulatory T cells. Eur J Appl Physiol 2013; 113(7): 1839-48.
[http://dx.doi.org/10.1007/s00421-013-2614-y] [PMID: 23435500]
[66]
Krüger K, Alack K, Ringseis R, Mink L, Pfeifer E, Schinle M. Apoptosis of t-cell subsets after acute high-intensity interval exercise. Med Sci Sports Exerc 2016; 48(10): 2021-9.
[67]
Dorneles GP, Haddad DO, Fagundes VO, et al. High intensity interval exercise decreases IL-8 and enhances the immunomodulatory cytokine interleukin-10 in lean and overweight-obese individuals. Cytokine 2016; 77: 1-9.
[http://dx.doi.org/10.1016/j.cyto.2015.10.003] [PMID: 26476404]
[68]
Dorneles GP, da Silva IRV, Korb A, et al. High intensity interval exercise enhances the global HDAC activity in PBMC and anti-inflammatory cytokines of overweight-obese subjects. Obes Med 2016; 2: 25-30.
[http://dx.doi.org/10.1016/j.obmed.2016.05.004]
[69]
Cabral-Santos C, de Lima Junior EA, Fernandes IMDC, et al. Interleukin-10 responses from acute exercise in healthy subjects: A systematic review. J Cell Physiol 2019; 234(7): 9956-65.
[http://dx.doi.org/10.1002/jcp.27920] [PMID: 30536945]
[70]
Bodor J, Bopp T, Vaeth M, et al. Cyclic AMP underpins suppression by regulatory T cells. Eur J Immunol 2012; 42(6): 1375-84.
[http://dx.doi.org/10.1002/eji.201141578] [PMID: 22678893]
[71]
Whiteside TL, Jackson EK. Adenosine and prostaglandin e2 production by human inducible regulatory T cells in health and disease. Front Immunol 2013; 4: 212.
[http://dx.doi.org/10.3389/fimmu.2013.00212] [PMID: 23898333]
[72]
Kuczma M, Lee JR, Kraj P. Connexin 43 signaling enhances the generation of Foxp3+ regulatory T cells. J Immunol 2011; 187(1): 248-57.
[http://dx.doi.org/10.4049/jimmunol.1003785] [PMID: 21642545]
[73]
Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 2010; 185(6): 3190-8.
[http://dx.doi.org/10.4049/jimmunol.0903670] [PMID: 20720200]
[74]
Yan Y, Zhang G-X, Gran B, et al. IDO upregulates regulatory T cells via tryptophan catabolite and suppresses encephalitogenic T cell responses in experimental autoimmune encephalomyelitis. J Immunol 2010; 185(10): 5953-61.
[http://dx.doi.org/10.4049/jimmunol.1001628] [PMID: 20944000]
[75]
Koliamitra C, Javelle F, Joisten N, et al. Do acute exercise-induced activations of the kynurenine pathway induce reg- ulatory T-Cells on the long-term? A theoretical frame work supported by pilot data. J Sports Sci Med 2019; 18(4): 669-73.
[76]
Minuzzi LG, Rama L, Bishop NC, et al. Lifelong training improves anti-inflammatory environment and maintains the number of regulatory T cells in masters athletes. Eur J Appl Physiol 2017; 117(6): 1131-40.
[http://dx.doi.org/10.1007/s00421-017-3600-6] [PMID: 28391394]
[77]
Dorneles GP, da Silva IM, Peres A, Romão PRT. Physical fitness modulates the expression of CD39 and CD73 on CD4+ CD25- and CD4+ CD25+ T cells following high intensity interval exercise. J Cell Biochem 2019; 120(6): 10726-36.
[http://dx.doi.org/10.1002/jcb.28364] [PMID: 30663116]
[78]
Mandapathil M, Hilldorfer B, Szczepanski MJ, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J Biol Chem 2010; 285(10): 7176-86.
[http://dx.doi.org/10.1074/jbc.M109.047423] [PMID: 19858205]
[79]
Dwyer KM, Deaglio S, Gao W, Friedman D, Strom TB, Robson SC. CD39 and control of cellular immune responses. Purinergic Signal 2007; 3(1-2): 171-80.
[http://dx.doi.org/10.1007/s11302-006-9050-y] [PMID: 18404431]
[80]
Linden J, Cekic C. Regulation of lymphocyte function by adenosine. Arterioscler Thromb Vasc Biol 2012; 32(9): 2097-103.
[http://dx.doi.org/10.1161/ATVBAHA.111.226837] [PMID: 22772752]
[81]
Clifford T, Wood MJ, Stocks P, Howatson G, Stevenson EJ, Hilkens CMU. T-regulatory cells exhibit a biphasic response to prolonged endurance exercise in humans. Eur J Appl Physiol 2017; 117(8): 1727-37.
[http://dx.doi.org/10.1007/s00421-017-3667-0] [PMID: 28646302]
[82]
Perry C, Pick M, Bdolach N, et al. Endurance exercise diverts the balance between Th17 cells and regulatory T cells. PLoS One 2013; 8(10)e74722
[http://dx.doi.org/10.1371/journal.pone.0074722] [PMID: 24130669]
[83]
Peake JM, Neubauer O, Della Gatta PA, Nosaka K. Muscle damage and inflammation during recovery from exercise. J Appl Physiol 2017; 122(3): 559-70.
[http://dx.doi.org/10.1152/japplphysiol.00971.2016] [PMID: 28035017]
[84]
Youngblood B, Hale JS, Ahmed R. T-cell memory differentiation: insights from transcriptional signatures and epigenetics. Immunology 2013; 139(3): 277-84.
[http://dx.doi.org/10.1111/imm.12074] [PMID: 23347146]
[85]
Schiaffino S, Pereira MG, Ciciliot S, Rovere-Querini P. Regulatory T cells and skeletal muscle regeneration. FEBS J 2017; 284(4): 517-24.
[http://dx.doi.org/10.1111/febs.13827] [PMID: 27479876]
[86]
Bianco TM, Abdalla DR, Desidério CS, et al. The influence of physical activity in the anti-tumor immune response in experimental breast tumor. Immunol Lett 2017; 190: 148-58.
[http://dx.doi.org/10.1016/j.imlet.2017.08.007] [PMID: 28818640]
[87]
Hagar A, Wang Z, Koyama S, et al. Endurance training slows breast tumor growth in mice by suppressing Treg cells recruitment to tumors. BMC Cancer 2019; 19(1): 536.
[http://dx.doi.org/10.1186/s12885-019-5745-7] [PMID: 31164094]
[88]
Lowder T, Dugger K, Deshane J, Estell K, Schwiebert LM. Repeated bouts of aerobic exercise enhance regulatory T cell responses in a murine asthma model. Brain Behav Immun 2010; 24(1): 153-9.
[http://dx.doi.org/10.1016/j.bbi.2009.09.011] [PMID: 19781626]
[89]
Fernandes P, de Mendonça Oliveira L, Brüggemann TR, Sato MN, Olivo CR, Arantes-Costa FM. Physical exercise induces immunoregulation of Treg, M2, and PDCs in a lung allergic inflammation model. Front Immunol 2019; 10: 854.
[http://dx.doi.org/10.3389/fimmu.2019.00854] [PMID: 31156611]
[90]
Dugger KJ, Chrisman T, Sayner SL, Chastain P, Watson K, Estes R. Beta-2 adrenergic receptors increase TREG cell suppression in an OVA-induced allergic asthma mouse model when mice are moderate aerobically exercised. BMC Immunol 2018; 19(1): 9.
[http://dx.doi.org/10.1186/s12865-018-0244-1] [PMID: 29452585]
[91]
Silva RA, Vieira RP, Duarte ACS, et al. Aerobic training reverses airway inflammation and remodelling in an asthma murine model. Eur Respir J 2010; 35(5): 994-1002.
[http://dx.doi.org/10.1183/09031936.00049509] [PMID: 19897558]
[92]
Uchiyama M, Jin X, Yin E, Shimokawa T, Niimi M. Treadmill exercise induces murine cardiac allograft survival and generates regulatory T cell. Transpl Int 2015; 28(3): 352-62.
[http://dx.doi.org/10.1111/tri.12491] [PMID: 25406375]
[93]
Rael VE, Chen L, McIntosh CM, Alegre ML. Exercise increases skin graft resistance to rejection. Am J Transplant 2019; 19(5): 1560-7.
[http://dx.doi.org/10.1111/ajt.15266] [PMID: 30659772]
[94]
Cook MD, Martin SA, Williams C, et al. Forced treadmill exercise training exacerbates inflammation and causes mortality while voluntary wheel training is protective in a mouse model of colitis. Brain Behav Immun 2013; 33: 46-56.
[http://dx.doi.org/10.1016/j.bbi.2013.05.005] [PMID: 23707215]
[95]
Souza PS, Gonçalves ED, Pedroso GS, et al. Physical exercise attenuates experimental autoimmune encephalomyelitis by inhibiting peripheral immune response and blood-brain barrier disruption. Mol Neurobiol 2017; 54(6): 4723-37.
[http://dx.doi.org/10.1007/s12035-016-0014-0] [PMID: 27447807]
[96]
Xie Y, Li Z, Wang Y, et al. Effects of moderate- versus high- intensity swimming training on inflammatory and CD4+ T cell subset profiles in experimental autoimmune encephalomyelitis mice. J Neuroimmunol 2019; 328: 60-7.
[http://dx.doi.org/10.1016/j.jneuroim.2018.12.005] [PMID: 30583216]
[97]
Wang J, Song H, Tang X, et al. Effect of exercise training intensity on murine T-regulatory cells and vaccination response. Scand J Med Sci Sports 2012; 22(5): 643-52.
[http://dx.doi.org/10.1111/j.1600-0838.2010.01288.x]
[98]
Schlittler M, Goiny M, Agudelo LZ, et al. Endurance exercise increases skeletal muscle kynurenine aminotransferases and plasma kynurenic acid in humans. Am J Physiol Cell Physiol 2016; 310(10): C836-40.
[http://dx.doi.org/10.1152/ajpcell.00053.2016] [PMID: 27030575]
[99]
Agudelo LZ, Ferreira DMS, Cervenka I, et al. Kynurenic acid and Gpr35 regulate adipose tissue energy homeostasis and inflammation. Cell Metab 2018; 27(2): 378-392: e5.
[http://dx.doi.org/10.1016/j.cmet.2018.01.004] [PMID: 29414686]
[100]
Hamaguchi M, Sakaguchi S. Regulatory T cells expressing PPAR-γ control inflammation in obesity. Cell Metab 2012; 16(1): 4-6.
[http://dx.doi.org/10.1016/j.cmet.2012.06.007] [PMID: 22768833]
[101]
Garf L, Murdaca J, Mothe-Satney I, et al. Complementary Immunometabolic Effects of exercise and PPAR β / δ agonist in the context of diet-induced weight loss in obese female mice. Int J Mol Sci 2019; 20(20): 5182.
[102]
Kolodin D, van Panhuys N, Li C, et al. Antigen- and cytokine-driven accumulation of regulatory T cells in visceral adipose tissue of lean mice. Cell Metab 2015; 21(4): 543-57.
[http://dx.doi.org/10.1016/j.cmet.2015.03.005] [PMID: 25863247]
[103]
Jakic B, Carlsson M, Buszko M, et al. The effects of endurance exercise and diet on atherosclerosis in young and aged ApoE-/- and wild-type mice. Gerontology 2019; 65(1): 45-56.
[http://dx.doi.org/10.1159/000492571] [PMID: 30165362]
[104]
Weinhold M, Shimabukuro-Vornhagen A, Franke A, et al. Physical exercise modulates the homeostasis of human regulatory T cells. J Allergy Clin Immunol 2016; 137(5): 1607-1610: e8.
[http://dx.doi.org/10.1016/j.jaci.2015.10.035] [PMID: 26774657]
[105]
Dorneles GP, da Silva I, Boeira MC, et al. Cardiorespiratory fitness modulates the proportions of monocytes and T helper subsets in lean and obese men. Scand J Med Sci Sports 2019; 29(11): 1-11.
[http://dx.doi.org/10.1111/sms.13506]
[106]
McRae JL, Chia JS, Pommey SA, Dwyer KM. Evaluation of CD4+ CD25+/- CD39+ T-cell populations in peripheral blood of patients following kidney transplantation and during acute allograft rejection. Nephrology (Carlton) 2017; 22(7): 505-12.
[http://dx.doi.org/10.1111/nep.12894] [PMID: 27517975]
[107]
Rehm K, Sunesara I, Marshall GD. Increased circulating anti-inflammatory cells in marathon-trained runners. Int J Sports Med 2015; 36(10): 832-6.
[http://dx.doi.org/10.1055/s-0035-1547218] [PMID: 26038877]
[108]
Dungey M, Young HML, Churchward DR, Burton JO, Smith AC, Bishop NC. Regular exercise during haemodialysis promotes an anti-inflammatory leucocyte profile. Clin Kidney J 2017; 10(6): 813-21.
[http://dx.doi.org/10.1093/ckj/sfx015] [PMID: 29225811]
[109]
Yeh SH, Chuang H, Lin LW, Hsiao CY, Wang PW, Yang KD. Tai chi chuan exercise decreases A1C levels along with increase of regulatory T-cells and decrease of cytotoxic T-cell population in type 2 diabetic patients. Diabetes Care 2007; 30(3): 716-8.
[http://dx.doi.org/10.2337/dc06-1507] [PMID: 17327347]
[110]
Yeh S-H, Lai H-L, Hsiao C-Y, et al. Moderate physical activity of music aerobic exercise increases lymphocyte counts, specific subsets, and differentiation. J Phys Act Health 2014; 11(7): 1386-92.
[http://dx.doi.org/10.1123/jpah.2012-0508]
[111]
Yeh SH, Chuang H, Lin LW, Hsiao CY, Eng HL. Regular tai chi chuan exercise enhances functional mobility and CD4CD25 regulatory T cells. Br J Sports Med 2006; 40(3): 239-43.
[http://dx.doi.org/10.1136/bjsm.2005.022095] [PMID: 16505081]
[112]
Yeh SH, Lai HL, Hsiao CY, et al. Moderate physical activity of music aerobic exercise increases lymphocyte counts, specific subsets, and differentiation. J Phys Act Health 2014; 11(7): 1386-92.
[http://dx.doi.org/10.1123/jpah.2012-0508]
[113]
Juszkiewicz A, Glapa A, Basta P, et al. The effect of L-theanine supplementation on the immune system of athletes exposed to strenuous physical exercise. J Int Soc Sports Nutr 2019; 16(1): 7.
[http://dx.doi.org/10.1186/s12970-019-0274-y] [PMID: 30770758]
[114]
Juszkiewicz A, Basta P, Petriczko E, et al. An attempt to induce an immunomodulatory effect in rowers with spirulina extract. J Int Soc Sports Nutr 2018; 15: 9.
[http://dx.doi.org/10.1186/s12970-018-0213-3] [PMID: 29467598]
[115]
Yeh SH, Chuang H, Lin LW, et al. Regular Tai Chi Chuan exercise improves T cell helper function of patients with type 2 diabetes mellitus with an increase in T-bet transcription factor and IL-12 production. Br J Sports Med 2009; 43(11): 845-50.
[http://dx.doi.org/10.1136/bjsm.2007.043562] [PMID: 18385192]
[116]
Momesso dos Santos CM, Sato FT, Cury-Boaventura MF, et al. Effect of regular circus physical exercises on lymphocytes in overweight children. PLoS One 2015; 10(3)e0120262
[http://dx.doi.org/10.1371/journal.pone.0120262] [PMID: 25826263]
[117]
Oderup C, Cederbom L, Makowska A, Cilio CM, Ivars F. Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression. Immunology 2006; 118(2): 240-9.
[http://dx.doi.org/10.1111/j.1365-2567.2006.02362.x] [PMID: 16771859]
[118]
Mähler A, Balogh A, Csizmadia I, et al. Metabolic, mental and immunological effects of normoxic and hypoxic training in multiple sclerosis patients: a pilot study. Front Immunol 2018; 9: 2819.
[http://dx.doi.org/10.3389/fimmu.2018.02819] [PMID: 30555484]

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