Frequent participation in high volume exercise throughout life is associated with a more differentiated adaptive immune response

Brain, Behavior, and Immunity

Volumn 39, Issue , 2014, Pages 61-74

  Moro García, Marco Antonio ^a   Fernández García, Benjamín ^b   Echeverría, Ainara ^a   Rodríguez Alonso, Manuel ^c   Suárez García, Francisco Manuel ^d   Solano Jaurrieta, Juan José ^e   López Larrea, Carlos ^a,f   Alonso Arias, Rebeca ^a  

^a HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^b UNIVERSITY OF OVIEDO   (Spain)

^c Instituto Vida Sana Balneario de las Caldas   (Spain)

^d Consejería de Salud y Servicios Sanitarios del Principado de Asturias ^*  (Spain)

^e HOSPITAL MONTE NARANCO   (Spain)

^f Section of Nephrology   (Spain)

Author keywords

Aging; Exercise; Lymphocyte differentiation; NK cells; T lymphocytes

Indexed keywords

ADAPTIVE IMMUNITY; ADULT; ANTIBODY TITER; ARTICLE; ATHLETE; BLOOD; BLOOD CELL COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CONTROLLED STUDY; DEGRANULATION; EXERCISE; FEMALE; FLOW CYTOMETRY; FUNCTIONAL STATUS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; LEUKOCYTE; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MALE; NATURAL KILLER CELL; NEUTROPHIL; NORMAL HUMAN; PHENOTYPE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; AGED; AGING; CYTOMEGALOVIRUS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; THYMUS;

ADAPTIVE IMMUNITY; ADULT; AGED; AGING; CYTOMEGALOVIRUS; EXERCISE; FEMALE; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTES; MALE; THYMUS GLAND;

EID: 84902341463     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.12.014     Document Type: Article

References (61)

1. Alonso-Arias R., Moro-Garcia M.A., Lopez-Vazquez A., Rodrigo L., Baltar J., Garcia F.M., Jaurrieta J.J., Lopez-Larrea C. NKG2D expression in CD4+ T lymphocytes as a marker of senescence in the aged immune system. Age (Dordr) 2011, 33:591-605.
2. Alonso-Arias R., Moro-García M.A., Echeverría A., Solano-Jaurrieta J.J., Suárez-García F.M., López-Larrea C. Intensity of the humoral response to cytomegalovirus is associated with the phenotypic and functional status of the immune system. J. Virol. 2013, 87:4486-4495.
3. Baj Z., Kantorski J., Majewska E., Zeman K., Pokoca L., Fornalczyk E., Tchorzewski H., Sulowska Z., Lewicki R. Immunological status of competitive cyclists before and after the training season. Int. J. Sports Med. 1994, 15:319-324.
4. Bauer M.E., Jeckel C.M., Luz C. The role of stress factors during aging of the immune system. Ann. N. Y. Acad. Sci. 2009, 1153:139-152.
5. Braith R.W., Stewart K.J. Resistance exercise training: its role in the prevention of cardiovascular disease. Circulation 2006, 113:2642-2650.
6. Clambey E.T., van Dyk L.F., Kappler J.W., Marrack P. Non-malignant clonal expansions of CD8+ memory T cells in aged individuals. Immunol. Rev. 2005, 205:170-189.
7. Cosgrove C., Galloway S.D., Neal C., Hunter A.M., McFarlin B.K., Spielmann G., Simpson R.J. The impact of 6-month training preparation for an Ironman triathlon on the proportions of naive, memory and senescent T cells in resting blood. Eur. J. Appl. Physiol. 2012, 112:2989-2998.
8. Cox A.J., Gleeson M., Pyne D.B., Callister R., Hopkins W.G., Fricker P.A. Clinical and laboratory evaluation of upper respiratory symptoms in elite athletes. Clin. J. Sport Med.: Off. J. Can. Acad. Sport Med. 2008, 18:438-445.
9. Czesnikiewicz-Guzik M., Lee W.W., Cui D., Hiruma Y., Lamar D.L., Yang Z.Z., Ouslander J.G., Weyand C.M., Goronzy J.J. T cell subset-specific susceptibility to aging. Clin. Immunol. 2008, 127:107-118.
10. Dons'koi B.V., Chernyshov V.P., Osypchuk D.V. Measurement of NK activity in whole blood by the CD69 up-regulation after co-incubation with K562, comparison with NK cytotoxicity assays and CD107a degranulation assay. J. Immunol. Methods 2011, 372:187-195.
11. Douek D.C., McFarland R.D., Keiser P.H., Gage E.A., Massey J.M., Haynes B.F., Polis M.A., Haase A.T., Feinberg M.B., Sullivan J.L., Jamieson B.D., Zack J.A., Picker L.J., Koup R.A. Changes in thymic function with age and during the treatment of HIV infection. Nature 1998, 396:690-695.
12. Franceschi C., Bonafe M., Valensin S., Olivieri F., De Luca M., Ottaviani E., De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 2000, 908:244-254.
13. Gleeson M., Bishop N.C. The T cell and NK cell immune response to exercise. Ann. Transplant. 2005, 10:43-48.
14. Gleeson M., Bishop N.C., Stensel D.J., Lindley M.R., Mastana S.S., Nimmo M.A. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat. Rev. Immunol. 2011, 11:607-615.
15. Hambrecht R., Wolf A., Gielen S., Linke A., Hofer J., Erbs S., Schoene N., Schuler G. Effect of exercise on coronary endothelial function in patients with coronary artery disease. N. Engl. J. Med. 2000, 342:454-460.
16. Helenius I., Lumme A., Haahtela T. Asthma, airway inflammation and treatment in elite athletes. Sports Med. 2005, 35:565-574.
17. Horn P.L., Pyne D.B., Hopkins W.G., Barnes C.J. Lower white blood cell counts in elite athletes training for highly aerobic sports. Eur. J. Appl. Physiol. 2010, 110:925-932.
18. Jackson A.S., Blair S.N., Mahar M.T., Wier L.T., Ross R.M., Stuteville J.E. Prediction of functional aerobic capacity without exercise testing. Med. Sci. Sports Exerc. 1990, 22:863-870.
19. Jadeski L., Hoffman-Goetz L. Exercise and in vivo natural cytotoxicity against tumour cells of varying metastatic capacity. Clin. Exp. Metastasis 1996, 14:138-144.
20. Kimmig S., Przybylski G.K., Schmidt C.A., Laurisch K., Mowes B., Radbruch A., Thiel A. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 2002, 195:789-794.
21. Koch S., Larbi A., Derhovanessian E., Ozcelik D., Naumova E., Pawelec G. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun. Ageing 2008, 5:6.
22. Lancaster G.I., Halson S.L., Khan Q., Drysdale P., Wallace F., Jeukendrup A.E., Drayson M.T., Gleeson M. Effects of acute exhaustive exercise and chronic exercise training on type 1 and type 2 T lymphocytes. Exerc. Immunol. Rev. 2004, 10:91-106.
23. Lee N., Goodlett D.R., Ishitani A., Marquardt H., Geraghty D.E. HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. 1998, 160:4951-4960.
24. Looney R.J., Falsey A., Campbell D., Torres A., Kolassa J., Brower C., McCann R., Menegus M., McCormick K., Frampton M., Hall W., Abraham G.N. Role of cytomegalovirus in the T cell changes seen in elderly individuals. Clin. Immunol. 1999, 90:213-219.
25. Lynch H.E., Goldberg G.L., Chidgey A., Van den Brink M.R., Boyd R., Sempowski G.D. Thymic involution and immune reconstitution. Trends Immunol. 2009, 30:366-373.
26. Mackinnon L.T., Hooper S.L. Plasma glutamine and upper respiratory tract infection during intensified training in swimmers. Med. Sci. Sports Exerc. 1996, 28:285-290.
27. Mahoney F.I., Barthel D.W. Functional evaluation: the Barthel Index. Md State Med. J. 1965, 14:61-65.
28. Manini T.M., Everhart J.E., Patel K.V., Schoeller D.A., Colbert L.H., Visser M., Tylavsky F., Bauer D.C., Goodpaster B.H., Harris T.B. Daily activity energy expenditure and mortality among older adults. JAMA 2006, 296:171-179.
29. Matthews C.E., Ockene I.S., Freedson P.S., Rosal M.C., Merriam P.A., Hebert J.R. Moderate to vigorous physical activity and risk of upper-respiratory tract infection. Med. Sci. Sports Exerc. 2002, 34:1242-1248.
30. McFarlin B.K., Flynn M.G., Phillips M.D., Stewart L.K., Timmerman K.L. Chronic resistance exercise training improves natural killer cell activity in older women. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:1315-1318.
31. Moro-Garcia M.A., Alonso-Arias R., Lopez-Vazquez A., Suarez-Garcia F.M., Solano-Jaurrieta J.J., Baltar J., Lopez-Larrea C. Relationship between functional ability in older people, immune system status, and intensity of response to CMV. Age (Dordr) 2012, 34:479-495.
32. Nieman D.C. Exercise, infection, and immunity. Int. J. Sports Med. 1994, 15(Suppl. 3):S131-S141.
33. Olsson J., Wikby A., Johansson B., Lofgren S., Nilsson B.O., Ferguson F.G. Age-related change in peripheral blood T-lymphocyte subpopulations and cytomegalovirus infection in the very old: the Swedish longitudinal OCTO immune study. Mech. Ageing Dev. 2000, 121:187-201.
34. Peake J., Nosaka K., Suzuki K. Characterization of inflammatory responses to eccentric exercise in humans. Exerc. Immunol. Rev. 2005, 11:64-85.
35. Peake J.M. Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc. Immunol. Rev. 2002, 8:49-100.
36. Peake J.M., Suzuki K., Wilson G., Hordern M., Nosaka K., Mackinnon L., Coombes J.S. Exercise-induced muscle damage, plasma cytokines, and markers of neutrophil activation. Med. Sci. Sports Exerc. 2005, 37:737-745.
37. Petersen A.M., Pedersen B.K. The anti-inflammatory effect of exercise. J. Appl. Physiol. 2005, 98:1154-1162.
38. Reid V.L., Gleeson M., Williams N., Clancy R.L. Clinical investigation of athletes with persistent fatigue and/or recurrent infections. Br. J. Sports Med. 2004, 38:42-45.
39. Roberts V., Maddison R., Simpson C., Bullen C., Prapavessis H. The acute effects of exercise on cigarette cravings, withdrawal symptoms, affect, and smoking behaviour: systematic review update and meta-analysis. Psychopharmacology 2012, 222:1-15.
40. Robson P.J., Blannin A.K., Walsh N.P., Castell L.M., Gleeson M. Effects of exercise intensity, duration and recovery on in vitro neutrophil function in male athletes. Int. J. Sports Med. 1999, 20:128-135.
41. Romeo J., Jimenez-Pavon D., Cervantes-Borunda M., Warnberg J., Gomez-Martinez S., Castillo M.J., Marcos A. Immunological changes after a single bout of moderate-intensity exercise in a hot environment. J. Physiol. Biochem. 2008, 64:197-204.
42. Rufer N., Zippelius A., Batard P., Pittet M.J., Kurth I., Corthesy P., Cerottini J.C., Leyvraz S., Roosnek E., Nabholz M., Romero P. Ex vivo characterization of human CD8+ T subsets with distinct replicative history and partial effector functions. Blood 2003, 102:1779-1787.
43. Sallusto F., Lenig D., Forster R., Lipp M., Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999, 401:708-712.
44. Shek P.N., Sabiston B.H., Buguet A., Radomski M.W. Strenuous exercise and immunological changes: a multiple-time-point analysis of leukocyte subsets, CD4/CD8 ratio, immunoglobulin production and NK cell response. Int. J. Sports Med. 1995, 16:466-474.
45. Simanek A.M., Dowd J.B., Pawelec G., Melzer D., Dutta A., Aiello A.E. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 2011, 6:e16103.
46. Simpson R.J., Lowder T.W., Spielmann G., Bigley A.B., LaVoy E.C., Kunz H. Exercise and the aging immune system. Ageing Res. Rev. 2012, 11:404-420.
47. Smithey M.J., Li G., Venturi V., Davenport M.P., Nikolich-Zugich J. Lifelong persistent viral infection alters the naive T cell pool, impairing CD8 T cell immunity in late life. J. Immunol. 2012, 189:5356-5366.
48. Speelman A.D., van de Warrenburg B.P., van Nimwegen M., Petzinger G.M., Munneke M., Bloem B.R. How might physical activity benefit patients with Parkinson disease?. Nat. Rev. Neurol. 2011, 7:528-534.
49. Spielmann G., McFarlin B.K., O'Connor D.P., Smith P.J., Pircher H., Simpson R.J. Aerobic fitness is associated with lower proportions of senescent blood T-cells in man. Brain Behav. Immun. 2011, 25:1521-1529.
50. Strandberg T.E., Pitkala K.H., Tilvis R.S. Cytomegalovirus antibody level and mortality among community-dwelling older adults with stable cardiovascular disease. JAMA 2009, 301:380-382.
51. Strindhall J., Nilsson B.O., Lofgren S., Ernerudh J., Pawelec G., Johansson B., Wikby A. No Immune Risk Profile among individuals who reach 100 years of age: findings from the Swedish NONA immune longitudinal study. Exp. Gerontol. 2007, 42:753-761.
52. Thompson P.D., Buchner D., Pina I.L., Balady G.J., Williams M.A., Marcus B.H., Berra K., Blair S.N., Costa F., Franklin G.F., Gordon N.F., Pate R.R., Rodriguez B.L., Yancey A.K., Wenger N.K. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation 2003, 107:3109-3116.
53. Timmons B.W., Cieslak T. Human natural killer cell subsets and acute exercise: a brief review. Exerc. Immunol. Rev. 2008, 14:8-23.
54. Turner J.E., Campbell J.P., Edwards K.M., Howarth L.J., Pawelec G., Aldred S., Moss P., Drayson M.T., Burns V.E., Bosch J.A. Rudimentary signs of immunosenescence in Cytomegalovirus-seropositive healthy young adults. Age (Dordr) 2013.
55. van Lier R.A., ten Berge I.J., Gamadia L.E. Human CD8(+) T-cell differentiation in response to viruses. Nat. Rev. Immunol. 2003, 3:931-939.
56. Walsh N.P., Gleeson M., Shephard R.J., Woods J.A., Bishop N.C., Fleshner M., Green C., Pedersen B.K., Hoffman-Goetz L., Rogers C.J., Northoff H., Abbasi A., Simon P. Position statement. Part one: immune function and exercise. Exerc. Immunol. Rev. 2011, 17:6-63.
57. Wang J.S., Weng T.P. Hypoxic exercise training promotes antitumour cytotoxicity of natural killer cells in young men. Clin. Sci. (Lond) 2011, 121:343-353.
58. Wikby A., Maxson P., Olsson J., Johansson B., Ferguson F.G. Changes in CD8 and CD4 lymphocyte subsets, T cell proliferation responses and non-survival in the very old: the Swedish longitudinal OCTO-immune study. Mech. Ageing Dev. 1998, 102:187-198.
59. Woods J.A., Ceddia M.A., Wolters B.W., Evans J.K., Lu Q., McAuley E. Effects of 6months of moderate aerobic exercise training on immune function in the elderly. Mech. Ageing Dev. 1999, 109:1-19.
60. Woods J.A., Davis J.M., Smith J.A., Nieman D.C. Exercise and cellular innate immune function. Med. Sci. Sports Exerc. 1999, 31:57-66.
61. Yang X.J., Hill K., Moore K., Williams S., Dowson L., Borschmann K., Simpson J.A., Dharmage S.C. Effectiveness of a targeted exercise intervention in reversing older people's mild balance dysfunction: a randomized controlled trial. Phys. Ther. 2012, 92:24-37.