Latent Cytomegalovirus infection amplifies CD8 T-lymphocyte mobilisation and egress in response to exercise

Brain, Behavior, and Immunity

Volumn 24, Issue 8, 2010, Pages 1362-1370

  Turner, James E ^a   Aldred, Sarah ^a   Witard, Oliver C ^a   Drayson, Mark T ^a   Moss, Paul M ^a   Bosch, Jos A ^a,b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

CD8+ T lymphocytes; Cytomegalovirus; Exercise; Human; Immune surveillance; Lymphocytopenia; Lymphocytosis; Memory lymphocytes; Migration; Stress

Indexed keywords

CD27 ANTIGEN; CD28 ANTIGEN; CD45RA ANTIGEN;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL MOTILITY; CELLULAR DISTRIBUTION; CYTOMEGALOVIRUS INFECTION; EFFECTOR CELL; EXERCISE; FLOW CYTOMETRY; HUMAN; HUMAN EXPERIMENT; IMMUNOCOMPETENT CELL; MALE; MEMORY CELL; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; TREADMILL EXERCISE;

ADULT; ANAEROBIC THRESHOLD; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS INFECTIONS; EXERCISE; EXERCISE TEST; FLOW CYTOMETRY; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOLOGIC SURVEILLANCE; LYMPHOCYTE COUNT; MALE; VIRUS LATENCY;

EID: 77957240274     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.07.239     Document Type: Article

References (76)

1. Ainsworth B.E., Haskell W.L., Leon A.S., Jacobs D.R., Montoye H.J., Sallis J.F., Paffenbarger R.S. Compendium of physical activities: classification of energy costs of human physical activities. Med. Sci. Sports Exerc. 1993, 25:71-80.
2. Ali S., O'Boyle G., Mellor P., Kirby J.A. An apparent paradox: chemokine receptor agonists can be used for anti-inflammatory therapy. Mol. Immunol. 2007, 44:1477-1482.
3. Anane L.H., Edwards K.M., Burns V.E., Drayson M.T., Riddell N.E., van Zanten J.J.C.S.V., Wallace G.R., Mills P.J., Bosch J.A. Mobilization of [gamma][delta] T lymphocytes in response to psychological stress, exercise, and [beta]-agonist infusion. Brain Behav. Immun. 2009, 23:823-829.
4. Appay V., Dunbar P.R., Callan M., Klenerman P., Gillespie G.M., Papagno L., Ogg G.S., King A., Lechner F., Spina C.A., Little S., Havlir D.V., Richman D.D., Gruener N., Pape G., Waters A., Easterbrook P., Salio M., Cerundolo V., McMichael A.J., Rowland-Jones S.L. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 2002, 8:379-385.
5. Appay V., van Lier R.A., Sallusto F., Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 2008, 73:975-983.
6. Benschop R.J., Nijkamp F.P., Ballieux R.E., Heijnen C.J. The effects of beta-adrenoceptor stimulation on adhesion of human natural killer cells to cultured endothelium. Br. J. Pharmacol. 1994, 113:1311-1316.
7. Borg G. Percieved exertion: a note on history and methods. Med. Sci. Sports Exerc. 1973, 5:90-93.
8. Burns L.J., Pooley J.C., Walsh D.J., Vercellotti G.M., Weber M.L., Kovacs A. Intercellular adhesion molecule-1 expression in endothelial cells is activated by cytomegalovirus immediate early proteins. Transplantation 1999, 67:137-144.
9. Campbell J.P., Guy K., Cosgrove C., Florida-James G.D., Simpson R.J. 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. 2008, 22:375-380.
10. Campbell J.P., Riddell N.E., Burns V.E., Turner M., van Zanten J.J.C.S.V., Drayson M.T., Bosch J.A. Acute exercise mobilises CD8+ T lymphocytes exhibiting an effector-memory phenotype. Brain Behav. Immun. 2009, 23:767-775.
11. Ceddia M.A., Price E.A., Kohlmeier C.K., Evans J.K., Lu Q., McAuley E., Woods J.A. Differential leukocytosis and lymphocyte mitogenic response to acute maximal exercise in the young and old. Med. Sci. Sports Exerc. 1999, 31:829-836.
12. Chidrawar S., Khan N., Wei W., McLarnon A., Smith N., Nayak L., Moss P. Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin. Exp. Immunol. 2009, 155:423-432.
13. Craig C.L., Marshall A.L., Sjostrom M., Bauman A.E., Booth M.L., Ainsworth B.E., Pratt M., Ekelund U., Yngve A., Sallis J.F., Oja P. International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc. 2003, 35:1381-1395.
14. Craigen J.L., Yong K.L., Jordan N.J., MacCormac L.P., Westwick J., Akbar A.N., Grundy J.E. Human cytomegalovirus infection up-regulates interleukin-8 gene expression and stimulates neutrophil transendothelial migration. Immunology 1997, 92:138-145.
15. de Boer O.J., Becker A.E., van der Wal A.C. T lymphocytes in atherogenesis-functional aspects and antigenic repertoire. Cardiovasc. Res. 2003, 60:78-86.
16. de Boer O.J., van der Wal A.C., Verhagen C.E., Becker A.E. Cytokine secretion profiles of cloned T cells from human aortic atherosclerotic plaques. J. Pathol. 1999, 188:174-179.
17. Dhabhar F.S. Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann. N. Y. Acad. Sci. 2000, 917:876-893.
18. Dhabhar F.S. Stress-induced augmentation of immune function - the role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav. Immun. 2002, 16:785-798.
19. Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. Effects of stress on immune cell distribution. Dynamics and hormonal mechanisms. J. Immunol. 1995, 154:5511-5527.
20. Dhabhar F.S., Miller A.H., McEwen B.S., Spencer R.L. Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. J. Immunol. 1996, 157:1638-1644.
21. Dimitrov S., Benedict C., Heutling D., Westermann J., Born J., Lange T. Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. Blood 2009, 113:5134-5143.
22. Dimitrov S., Lange T., Born J. Selective mobilization of cytotoxic leukocytes by epinephrine. J. Immunol. 2010, 184:503-511.
23. Dowd J.B., Aiello A.E. Socioeconomic differentials in immune response. Epidemiology 2009, 20:902-908.
24. Dumortier J., Streblow D.N., Moses A.V., Jacobs J.M., Kreklywich C.N., Camp D., Smith R.D., Orloff S.L., Nelson J.A. Human cytomegalovirus secretome contains factors that induce angiogenesis and wound healing. J. Virol. 2008, 82:6524-6535.
25. Edwards K.M., Burns V.E., Allen L.M., McPhee J.S., Bosch J.A., Carroll D., Drayson M., Ring C. Eccentric exercise as an adjuvant to influenza vaccination in humans. Brain Behav. Immun. 2007, 21:209-217.
26. Edwards K.M., Burns V.E., Reynolds T., Carroll D., Drayson M., Ring C. Acute stress exposure prior to influenza vaccination enhances antibody response in women. Brain Behav. Immun. 2006, 20:159-168.
27. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 2000, 52:595-638.
28. Fauci A.S. Mechanisms of corticosteroid action on lymphocyte subpopulations. II. Differential effects of in vivo hydrocortisone, prednisone and dexamethasone on in vitro expression of lymphocyte function. Clin. Exp. Immunol. 1976, 24:54-62.
29. Fisher J.P., Young C.N., Fadel P.J. Central sympathetic overactivity: maladies and mechanisms. Auton. Neurosci. 2009, 148:5-15.
30. Fletcher J.M., Vukmanovic-Stejic M., Dunne P.J., Birch K.E., Cook J.E., Jackson S.E., Salmon M., Rustin M.H., Akbar A.N. Cytomegalovirus-specific CD4+ T cells in healthy carriers are continuously driven to replicative exhaustion. J. Immunol. 2005, 175:8218-8225.
31. Gewaltig J., Kummer M., Koella C., Cathomas G., Biedermann B.C. Requirements for CD8 T-cell migration into the human arterial wall. Hum. Pathol. 2008, 39:1756-1762.
32. Gleeson M., Bishop N.C. The T cell and NK cell immune response to exercise. Ann. Transplant. 2005, 10:43-48.
33. Hadrup S.R., Strindhall J., Kollgaard T., Seremet T., Johansson B., Pawelec G., thor Straten P., Wikby A. Longitudinal studies of clonally expanded CD8 T cells reveal a repertoire shrinkage predicting mortality and an increased number of dysfunctional cytomegalovirus-specific T cells in the very elderly. J. Immunol. 2006, 176:2645-2653.
34. Hamann D., Baars P.A., Rep M.H., Hooibrink B., Kerkhof-Garde S.R., Klein M.R., van Lier R.A. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 1997, 186:1407-1418.
35. Hansen J.B., Wilsgard L., Osterud B. Biphasic changes in leukocytes induced by strenuous exercise. Eur. J. Appl. Physiol. Occup. Physiol. 1991, 62:157-161.
36. Holmes S., He M., Xu T., Lee P.P. Memory T cells have gene expression patterns intermediate between naive and effector. Proc. Natl. Acad. Sci. USA 2005, 102:5519-5523.
37. Hong S., Farag N.H., Nelesen R.A., Ziegler M.G., Mills P.J. Effects of regular exercise on lymphocyte subsets and CD62L after psychological vs. physical stress. J. Psychosom. Res. 2004, 56:363-370.
38. Hong S., Johnson T.A., Farag N.H., Guy H.J., Matthews S.C., Ziegler M.G., Mills P.J. Attenuation of T-lymphocyte demargination and adhesion molecule expression in response to moderate exercise in physically fit individuals. J. Appl. Physiol. 2005, 98:1057-1063.
39. Jennings J.R., Stine L.A. Salient method, design and analysis concerns. Handbook of Psychophysiology 2007, 870-899. Cambridge University Press, Cambridge, UK. J.T. Cacioppo, L.G. Tassinary, G.G. Berntson (Eds.).
40. Karaszewski J.W., Reder A.T., Anlar B., Kim W.C., Arnason B.G. Increased lymphocyte beta-adrenergic receptor density in progressive multiple sclerosis is specific for the CD8+, CD28- suppressor cell. Ann. Neurol. 1991, 30:42-47.
41. Khan N., Shariff N., Cobbold M., Bruton R., Ainsworth J.A., Sinclair A.J., Nayak L., Moss P.A. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 2002, 169:1984-1992.
42. Krüger K., Lechtermann A., Fobker M., Völker K., Mooren F.C. Exercise-induced redistribution of T lymphocytes is regulated by adrenergic mechanisms. Brain Behav. Immun. 2008, 22:324-338.
43. Krüger K., Mooren F.C. T cell homing and exercise. Exerc. Immunol. Rev. 2007, 13:37-54.
44. Kuhlwein E.C., Irwin M.R., Ziegler M.G., Woods V.L., Kennedy B., Mills P.J. Propranolol affects stress-induced leukocytosis and cellular adhesion molecule expression. Eur. J. Appl. Physiol. 2001, 86:135-141.
45. Lubeck P.R., Doerr H.W., Rabenau H.F. Epidemiology of human cytomegalovirus (HCMV) in an urban region of Germany: what has changed?. Med. Microbiol. Immunol. 2010, 199:53-60.
46. Mars M., Govender S., Weston A., Naicker V., Chuturgoon A. High intensity exercise: a cause of lymphocyte apoptosis?. Biochem. Biophys. Res. Commun. 1998, 249:366-370.
47. Mazzeo R.S., Rajkumar C., Rolland J., Blaher B., Jennings G., Esler M. Immune response to a single bout of exercise in young and elderly subjects. Mech. Ageing Dev. 1998, 100:121-132.
48. McCarthy D.A., Dale M.M. The leucocytosis of exercise. Sports Med. 1988, 6:333-363.
49. Mills P.J., Farag N.H., Hong S., Kennedy B.P., Berry C.C., Ziegler M.G. Immune cell CD62L and CD11a expression in response to a psychological stressor in human hypertension. Brain Behav. Immun. 2003, 17:260-267.
50. Mills P.J., Hong S., Redwine L., Carter S.M., Chiu A., Ziegler M.G., Dimsdale J.E., Maisel A.S. Physical fitness attenuates leukocyte-endothelial adhesion in response to acute exercise. J. Appl. Physiol. 2006, 101:785-788.
51. Mills P.J., Rehman J., Ziegler M.G., Carter S.M., Dimsdale J.E., Maisel A.S. Nonselective beta blockade attenuates the recruitment of CD62L(-)T lymphocytes following exercise. Eur. J. Appl. Physiol. Occup. Physiol. 1999, 79:531-534.
52. Mooren F.C., Bloming D., Lechtermann A., Lerch M.M., Volker K. Lymphocyte apoptosis after exhaustive and moderate exercise. J. Appl. Physiol. 2002, 93:147-153.
53. Mooren F.C., Lechtermann A., Volker K. Exercise-induced apoptosis of lymphocytes depends on training status. Med. Sci. Sports Exerc. 2004, 36:1476-1483.
54. Nieman D.C. Upper respiratory tract infections and exercise. Thorax 1995, 50:1229-1231.
55. 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.
56. Onsrud M., Thorsby E. Influence of in vivo hydrocortisone on some human blood lymphocyte subpopulations. I. Effect on natural killer cell activity. Scand. J. Immunol. 1981, 13:573-579.
57. Pedersen B.K., Hoffman-Goetz L. Exercise and the immune system: regulation, integration and adaptation. Physiol. Rev. 2000, 80:1055-1081.
58. Pourgheysari B., Khan N., Best D., Bruton R., Nayak L., Moss P.A. The cytomegalovirus-specific CD4+ T-cell response expands with age and markedly alters the CD4+ T-cell repertoire. J. Virol. 2007, 81:7759-7765.
59. Romero P., Zippelius A., Kurth I., Pittet M.J., Touvrey C., Iancu E.M., Corthesy P., Devevre E., Speiser D.E., Rufer N. Four functionally distinct populations of human effector-memory CD8+ T lymphocytes. J. Immunol. 2007, 178:4112-4119.
60. 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.
61. Shephard R.J., Shek P.N. Effects of exercise and training on natural killer cell counts and cytolytic activity: a meta-analysis. Sports Med. 1999, 28:177-195.
62. Shinkai S., Konishi M., Shephard R.J. Aging and immune response to exercise. Can. J. Physiol. Pharmacol. 1998, 76:562-572.
63. Simpson R.J., Cosgrove C., Ingram L.A., Florida-James G.D., Whyte G.P., Pircher H., Guy K. Senescent T-lymphocytes are mobilised into the peripheral blood compartment in young and older humans after exhaustive exercise. Brain Behav. Immun. 2008, 22:544-551.
64. Simpson R.J., Florida-James G.D., Cosgrove C., Whyte G.P., Macrae S., Pircher H., Guy K. High-intensity exercise elicits the mobilization of senescent T lymphocytes into the peripheral blood compartment in human subjects. J. Appl. Physiol. 2007, 103:396-401.
65. Simpson R.J., Florida-James G.D., Whyte G.P., Black J.R., Ross J.A., Guy K. Apoptosis does not contribute to the blood lymphocytopenia observed after intensive and downhill treadmill running in humans. Res. Sports Med. 2007, 15:157-174.
66. Staras S.A., Dollard S.C., Radford K.W., Flanders W.D., Pass R.F., Cannon M.J. Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin. Infect. Dis. 2006, 43:1143-1151.
67. Stowe R.P., Kozlova E.V., Yetman D.L., Walling D.M., Goodwin J.S., Glaser R. Chronic herpesvirus reactivation occurs in aging. Exp. Gerontol. 2007, 42:563-570.
68. Strandberg T.E., Pitkala K.H., Linnavuori K.H., Tilvis R.S. Impact of viral and bacterial burden on cognitive impairment in elderly persons with cardiovascular diseases. Stroke 2003, 34:2126-2131.
69. Streblow D.N., Dumortier J., Moses A.V., Orloff S.L., Nelson J.A. Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr. Top. Microbiol. Immunol. 2008, 325:397-415.
70. 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.
71. Tanimura Y., Shimizu K., Tanabe K., Otsuki T., Yamauchi R., Matsubara Y., Iemitsu M., Maeda S., Ajisaka R. Exercise-induced oxidative DNA damage and lymphocytopenia in sedentary young males. Med. Sci. Sports Exerc. 2008, 40:1455-1462.
72. 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.
73. Weinberger B., Lazuardi L., Weiskirchner I., Keller M., Neuner C., Fischer K.H., Neuman B., Wurzner R., Grubeck-Loebenstein B. Healthy aging and latent infection with CMV lead to distinct changes in CD8(+) and CD4(+) T-cell subsets in the elderly. Hum. Immunol. 2007, 68:86-90.
74. ACSM's Guidelines for Exercise Testing and Prescription 2006, Lippincott Williams and Wilkins, Baltimore, MD. M.H. Whaley, P.H. Brubaker, R.M. Otto (Eds.).
75. Wikby A., Johansson B., Olsson J., Lofgren S., Nilsson B.O., Ferguson F. Expansions of peripheral blood CD8 T-lymphocyte subpopulations and an association with cytomegalovirus seropositivity in the elderly: the Swedish NONA immune study. Exp. Gerontol. 2002, 37:445-453.
76. Zanghellini F., Boppana S.B., Emery V.C., Griffiths P.D., Pass R.F. Asymptomatic primary cytomegalovirus infection: virologic and immunologic features. J. Infect. Dis. 1999, 180:702-707.