Senescent phenotypes and telomere lengths of peripheral blood T-cells mobilized by acute exercise in humans

Exercise Immunology Review

Volumn 16, Issue , 2010, Pages 40-55

  Simpson, Richard J ^a,b   Cosgrove, Cormac ^b   Chee, Meng M ^c   McFarlin, Brian K ^a   Bartlett, David B ^a,b   Spielmann, Guillaume ^a,b   O'Connor, Daniel P ^a   Pircher, Hanspeter ^d   Shiels, Paul G ^c  

^a UNIVERSITY OF HOUSTON   (United States)

^b EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

CD28; CD57; Effector memory T cells; Exercise immunology; Immunosenescence; Killer cell lectin like receptor G1 (KLRG1); STASIS

Indexed keywords

CD28 ANTIGEN; CD3 ANTIBODY; CD3 ANTIGEN; CD4 ANTIBODY; CD57 ANTIGEN; CD8 ANTIGEN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; KLRG1 PROTEIN, HUMAN; LECTIN; TRANSACTIVATOR PROTEIN;

AEROBIC EXERCISE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL ISOLATION; CLINICAL PROTOCOL; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; PERIPHERAL LYMPHOCYTE; PHENOTYPE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SENESCENCE; STRESS; TELOMERE; TREADMILL EXERCISE; ADULT; BIOSYNTHESIS; CELL AGING; CELL MOTION; CELL SEPARATION; CYTOLOGY; EXERCISE; IMMUNOLOGY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ADULT; CELL AGING; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SEPARATION; EXERCISE; FLOW CYTOMETRY; HUMANS; LECTINS, C-TYPE; MALE; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; TELOMERE; TRANS-ACTIVATORS;

EID: 77957938521     PISSN: 10775552     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Anane LH, Edwards KM, Burns VE, Drayson MT, Riddell NE, van Zanten JJ, Wallace GR, Mills PJ, and Bosch JA. Mobilization of gammadelta T lymphocytes in response to psychological stress, exercise, and beta-agonist infusion. Brain Behav Immun 23: 823-829, 2009.
2. Atanackovic D, Schnee B, Schuch G, Faltz C, Schulze J, Weber CS, Schafhausen P, Bartels K, Bokemeyer C, Brunner-Weinzierl MC, and Deter HC. Acute psychological stress alerts the adaptive immune response: stress-induced mobilization of effector T cells. J Neuroimmunol 176: 141-152, 2006. (Pubitemid 44080330)
3. Brenchley JM, Karandikar NJ, Betts MR, Ambrozak DR, Hill BJ, Crotty LE, Casazza JP, Kuruppu J, Migueles SA, Connors M, Roederer M, Douek DC, and Koup RA. Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 101: 2711-2720, 2003. (Pubitemid 36857634)
4. Bruunsgaard H, Jensen MS, Schjerling P, Halkjaer-Kristensen J, Ogawa K, Skinhoj P, and Pedersen BK. Exercise induces recruitment of lymphocytes with an activated phenotype and short telomeres in young and elderly humans. Life Sci 65: 2623-2633, 1999.
5. Campbell JP, Guy K, Cosgrove C, Florida-James GD, and Simpson RJ. Total lymphocyte CD8 expression is not a reliable marker of cytotoxic T-cell populations in human peripheral blood following an acute bout of high-intensity exercise. Brain Behav Immun 22: 375-380, 2008. (Pubitemid 351172704)
6. Campbell JP, Riddell NE, Burns VE, Turner M, van Zanten JJ, Drayson MT, and Bosch JA. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effectormemory phenotype. Brain Behav Immun 23: 767-775, 2009.
7. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res 30: e47, 2002.
8. Grubeck-Loebenstein B, Della Bella S, Iorio AM, Michel JP, Pawelec G, and Solana R. Immunosenescence and vaccine failure in the elderly. Aging Clin Exp Res 21: 201-209, 2009.
9. Harris SE, Deary IJ, MacIntyre A, Lamb KJ, Radhakrishnan K, Starr JM, Whalley LJ, and Shiels PG. The association between telomere length, physical health, cognitive ageing, and mortality in non-demented older people. Neurosci Lett 406: 260- 264, 2006.
10. Henson SM, Franzese O, Macaulay R, Libri V, Azevedo RI, Kiani-Alikhan S, Plunkett FJ, Masters JE, Jackson S, Griffiths SJ, Pircher HP, Soares MV, and Akbar AN. KLRG1 signaling induces defective Akt (ser473) phosphorylation and proliferative dysfunction of highly differentiated CD8+ T cells. Blood 113: 6619-6628, 2009.
11. Hoffman-Goetz L, and Quadrilatero J. Treadmill exercise in mice increases intestinal lymphocyte loss via apoptosis. Acta Physiol Scand 179: 289-297, 2003. (Pubitemid 37464114)
12. Ibegbu CC, Xu YX, Harris W, Maggio D, Miller JD, and Kourtis AP. Expression of killer cell lectin-like receptor G1 on antigen-specific human CD8+ T lymphocytes during active, latent, and resolved infection and its relation with CD57. J Immunol 174: 6088-6094, 2005. (Pubitemid 40663797)
13. Koch S, Larbi A, Ozcelik D, Solana R, Gouttefangeas C, Attig S, Wikby A, Strindhall J, Franceschi C, and Pawelec G. Cytomegalovirus infection: a driving force in human T cell immunosenescence. Ann NY Acad Sci 1114: 23-35, 2007. (Pubitemid 350070409)
14. Koch S, Solana R, Dela Rosa O, and Pawelec G. Human cytomegalovirus infection and T cell immunosenescence: a mini review. Mech Ageing Dev 127: 538-543, 2006.
15. Kruger K, Lechtermann A, Fobker M, Volker K, and Mooren FC. Exercise-induced redistribution of T lymphocytes is regulated by adrenergic mechanisms. Brain Behav Immun 22: 324-338, 2008. (Pubitemid 351172699)
16. Kruger K, and Mooren FC. T cell homing and exercise. Exerc Immunol Rev 13: 37- 54, 2007.
17. Li Y, Hofmann M, Wang Q, Teng L, Chlewicki LK, Pircher H, and Mariuzza RA. Structure of natural killer cell receptor KLRG1 bound to E-cadherin reveals basis for MHC-independent missing self recognition. Immunity 31: 35-46, 2009.
18. Marcolino I, Przybylski GK, Koschella M, Schmidt CA, Voehringer D, Schlesier M, and Pircher H. Frequent expression of the natural killer cell receptor KLRG1 in human cord blood T cells: correlation with replicative history. Eur J Immunol 34: 2672-2680, 2004. (Pubitemid 39430144)
19. Mariani E, Meneghetti A, Formentini I, Neri S, Cattini L, Ravaglia G, Forti P, and Facchini A. Different rates of telomere shortening and telomerase activity reduction in CD8 T and CD16 NK lymphocytes with ageing. Exp Gerontol 38: 653-659, 2003. (Pubitemid 36694167)
20. Masopust D, Vezys V, Marzo AL, and Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417, 2001. (Pubitemid 32231804)
21. McFarlin BK, Flynn MG, Stewart LK, and Timmerman KL. Carbohydrate intake during endurance exercise increases natural killer cell responsiveness to IL-2. J Appl Physiol 96: 271-275, 2004. (Pubitemid 38032010)
22. Mooren FC, Bloming D, Lechtermann A, Lerch MM, and Volker K. Lymphocyte apoptosis after exhaustive and moderate exercise. J Appl Physiol 93: 147-153, 2002. (Pubitemid 34686205)
23. Nielsen HB, Secher NH, Kristensen JH, Christensen NJ, Espersen K, and Pedersen BK. Splenectomy impairs lymphocytosis during maximal exercise. Am J Physiol 272: R1847-1852, 1997.
24. Ouyang Q, Wagner WM, Voehringer D, Wikby A, Klatt T, Walter S, Muller CA, Pircher H, and Pawelec G. Age-associated accumulation of CMV-specific CD8+ T cells expressing the inhibitory killer cell lectin-like receptor G1 (KLRG1). Exp Gerontol 38: 911-920, 2003. (Pubitemid 36952673)
25. Pawelec G. Immunosenescence and vaccination. Immun Ageing 2: 16, 2005.
26. Pawelec G, Akbar A, Caruso C, Solana R, Grubeck-Loebenstein B, and Wikby A. Human immunosenescence: is it infectious? Immunol Rev 205: 257-268, 2005. (Pubitemid 40780191)
27. Pawelec G, Derhovanessian E, Larbi A, Strindhall J, and Wikby A. Cytomegalovirus and human immunosenescence. Rev Med Virol 19: 47-56, 2009.
28. Peters EM, Van Eden M, Tyler N, Ramautar A, and Chuturgoon AA. Prolonged exercise does not cause lymphocyte DNA damage or increased apoptosis in well-trained endurance athletes. Eur J Appl Physiol 98: 124-131, 2006. (Pubitemid 44349892)
29. Rosshart S, Hofmann M, Schweier O, Pfaff AK, Yoshimoto K, Takeuchi T, Molnar E, Schamel WW, and Pircher H. Interaction of KLRG1 with E-cadherin: new functional and structural insights. Eur J Immunol 38: 3354-3364, 2008.
30. Shay JW, and Roninson IB. Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 23: 2919-2933, 2004. (Pubitemid 38638853)
31. Shephard RJ. Adhesion molecules, catecholamines and leucocyte redistribution during and following exercise. Sports Med 33: 261-284, 2003. (Pubitemid 36433821)
32. Shinomiya N, Koike Y, Koyama H, Takayama E, Habu Y, Fukasawa M, Tanuma S, and Seki S. Analysis of the susceptibility of CD57 T cells to CD3-mediated apoptosis. Clin Exp Immunol 139: 268-278, 2005. (Pubitemid 40222844)
33. Simpson RJ, Cosgrove C, Ingram LA, Florida-James GD, Whyte GP, Pircher H, and Guy K. Senescent T-lymphocytes are mobilised into the peripheral blood compartment in young and older humans after exhaustive exercise. Brain Behav Immun 22: 544-551, 2008.
34. Simpson RJ, Florida-James GD, Cosgrove C, Whyte GP, Macrae S, Pircher H, and Guy K. High-intensity exercise elicits the mobilization of senescent T lymphocytes into the peripheral blood compartment in human subjects. J Appl Physiol 103: 396-401, 2007. (Pubitemid 47092317)
35. Simpson RJ, Florida-James GD,Whyte GP, Black JR, Ross JA, and Guy K. Apoptosis does not contribute to the blood lymphocytopenia observed after intensive and downhill treadmill running in humans. Res Sports Med 15: 157-174, 2007. (Pubitemid 350072561)
36. Simpson RJ, Florida-James GD, Whyte GP, and Guy K. The effects of intensive, moderate and downhill treadmill running on human blood lymphocytes expressing the adhesion/activation molecules CD54 (ICAM-1), CD18 (beta2 integrin) and CD53. Eur J Appl Physiol 97: 109-121, 2006. (Pubitemid 43949794)
37. Simpson RJ, and Guy K. Coupling Aging Immunity with a Sedentary Lifestyle: Has the Damage Already Been Done? - A Mini-Review. Gerontology 2009. PMID: 20029165
38. Simpson RJ, Wilson MR, Black JR, Ross JA, Whyte GP, Guy K, and Florida-James GD. Immune alterations, lipid peroxidation, and muscle damage following a hill race. Can J Appl Physiol 30: 196-211, 2005. (Pubitemid 40627543)
39. Spaulding C, Guo W, and Effros RB. Resistance to apoptosis in human CD8+ T cells that reach replicative senescence after multiple rounds of antigen-specific proliferation. Exp Gerontol 34: 633-644, 1999. (Pubitemid 29420328)
40. Starr JM, McGurn B, Harris SE, Whalley LJ, Deary IJ, and Shiels PG. Association between telomere length and heart disease in a narrow age cohort of older people. Exp Gerontol 42: 571-573, 2007. (Pubitemid 46756090)
41. Starr JM, Shiels PG, Harris SE, Pattie A, Pearce MS, Relton CL, and Deary IJ. Oxidative stress, telomere length and biomarkers of physical aging in a cohort aged 79 years from the 1932 Scottish Mental Survey. Mech Ageing Dev 2008.
42. Steensberg A, Morrow J, Toft AD, Bruunsgaard H, and Pedersen BK. Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur J Appl Physiol 87: 38-42, 2002. (Pubitemid 41399029)
43. Targonski PV, Jacobson RM, and Poland GA. Immunosenescence: role and measurement in influenza vaccine response among the elderly. Vaccine 25: 3066-3069, 2007. (Pubitemid 46482735)
44. Timmons BW, and Bar-Or O. Lymphocyte expression of CD95 at rest and in response to acute exercise in healthy children and adolescents. Brain Behav Immun 21: 442-449, 2007. (Pubitemid 46528678)
45. Van den Hove LE, Van Gool SW, Vandenberghe P, Boogaerts MA, and Ceuppens JL. CD57+/CD28- T cells in untreated hemato-oncological patients are expanded and display a Th1-type cytokine secretion profile, ex vivo cytolytic activity and enhanced tendency to apoptosis. Leukemia 12: 1573-1582, 1998. (Pubitemid 28470442)
46. Voehringer D, Blaser C, Brawand P, Raulet DH, Hanke T, and Pircher H. Viral infections induce abundant numbers of senescent CD8 T cells. J Immunol 167: 4838-4843, 2001. (Pubitemid 33009711)
47. Voehringer D, Koschella M, and Pircher H. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 100: 3698-3702, 2002 (Pubitemid 35303941)