Exercise enhances vaccine-induced antigen-specific T cell responses

Vaccine

Volumn 26, Issue 42, 2008, Pages 5407-5415

  Rogers, Connie J ^a   Zaharoff, David A ^a   Hance, Kenneth W ^a   Perkins, Susan N ^b   Hursting, Stephen D ^b,c   Schlom, Jeffrey ^a   Greiner, John W ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Adaptive immunity; Cell proliferation; Cytokines

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN G; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; LYMPHOTACTIN; OVALBUMIN; TUMOR NECROSIS FACTOR ALPHA; VACCINE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BODY COMPOSITION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXERCISE; FEMALE; FLOW CYTOMETRY; INGUINAL LYMPH NODE; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MESENTERY LYMPH NODE; MIXED LYMPHOCYTE REACTION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; REVACCINATION; SPLEEN CELL; T LYMPHOCYTE; TREADMILL; VACCINATION;

ANIMALS; BODY COMPOSITION; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOKINES; FEMALE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; OVALBUMIN; SUBSTRATE SPECIFICITY; VACCINATION;

EID: 51549096347     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2008.07.081     Document Type: Article

References (56)

1. Blair S.N., Cheng Y., and Holder J.S. Is physical activity or physical fitness more important in defining health benefits?. Med Sci Sports Exerc 33 6 Suppl (2001) S379-S399 discussion S419-20
2. Melzer K., Kayser B., and Pichard C. Physical activity: the health benefits outweigh the risks. Curr Opin Clin Nutr Metab Care 7 6 (2004) 641-647
3. Woods J.A., Davis J.M., Smith J.A., and Nieman D.C. Exercise and cellular innate immune function. Med Sci Sports Exerc 31 1 (1999) 57-66
4. Nieman D.C., Henson D.A., Gusewitch G., Warren B.J., Dotson R.C., Butterworth D.E., et al. Physical activity and immune function in elderly women. Med Sci Sports Exerc 25 7 (1993) 823-831
5. Matthews C.E., Ockene I.S., Freedson P.S., Rosal M.C., Merriam P.A., and Hebert J.R. Moderate to vigorous physical activity and risk of upper-respiratory tract infection. Med Sci Sports Exerc 34 8 (2002) 1242-1248
6. Cieslak T.J., Frost G., and Klentrou P. Effects of physical activity, body fat, and salivary cortisol on mucosal immunity in children. J Appl Physiol 95 6 (2003) 2315-2320
7. Chubak J., McTiernan A., Sorensen B., Wener M.H., Yasui Y., Velasquez M., et al. Moderate-intensity exercise reduces the incidence of colds among postmenopausal women. Am J Med 119 11 (2006) 937-942
8. Nieman D.C., Nehlsen-Cannarella S.L., Markoff P.A., Balk-Lamberton A.J., Yang H., Chritton D.B., et al. The effects of moderate exercise training on natural killer cells and acute upper respiratory tract infections. Int J Sports Med 11 6 (1990) 467-473
9. Nieman D.C., Nehlsen-Cannarella S.L., Henson D.A., Koch A.J., Butterworth D.E., Fagoaga O.R., et al. Immune response to exercise training and/or energy restriction in obese women. Med Sci Sports Exerc 30 5 (1998) 679-686
10. Kostka T., Berthouze S.E., Lacour J., and Bonnefoy M. The symptomatology of upper respiratory tract infections and exercise in elderly people. Med Sci Sports Exerc 32 1 (2000) 46-51
11. Strasner A., Barlow C.E.J.B., and Dunn K.A.L. Impact of physical activity on URTI symptoms in Project PRIME participants. Med Sci Sports Exerc 33 Suppl. (2001) S304
12. Klentrou P., Cieslak T., MacNeil M., Vintinner A., and Plyley M. Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans. Eur J Appl Physiol 87 2 (2002) 153-158
13. Cannon J.G., and Kluger M.J. Exercise enhances survival rate in mice infected with Salmonella typhimurium. Proc Soc Exp Biol Med 175 4 (1984) 518-521
14. Ilback N.G., Friman G., Beisel W.R., Johnson A.J., and Berendt R.F. Modifying effects of exercise on clinical course and biochemical response of the myocardium in influenza and tularemia in mice. Infect Immun 45 2 (1984) 498-504
15. Schouten W.J., Verschuur R., and Kemper H.C. Habitual physical activity, strenuous exercise, and salivary immunoglobulin A levels in young adults: the Amsterdam Growth and Health Study. Int J Sports Med 9 4 (1988) 289-293
16. Tharp G.D. Basketball exercise and secretory immunoglobulin A. Eur J Appl Physiol Occup Physiol 63 3-4 (1991) 312-314
17. Akimoto T., Kumai Y., Akama T., Hayashi E., Murakami H., Soma R., et al. Effects of 12 months of exercise training on salivary secretory IgA levels in elderly subjects. Br J Sports Med 37 1 (2003) 76-79
18. Rogers C.J., Berrigan D., Zaharoff D.A., Hance K.W., Patel A.C., Perkins S.N., et al. Energy restriction and exercise differentially enhance components of systemic and mucosal immunity in mice. J Nutr 138 1 (2008) 115-122
19. Woods J., Lu Q., Ceddia M.A., and Lowder T. Special feature for the Olympics: effects of exercise on the immune system: exercise-induced modulation of macrophage function. Immunol Cell Biol 78 5 (2000) 545-553
20. Hance K.W., Rogers C.J., Hursting S.D., and Greiner J.W. Combination of physical activity, nutrition, or other metabolic factors and vaccine response. Front Biosci 12 (2007) 4997-5029
21. Keylock K.T., Lowder T., Leifheit K.A., Cook M., Mariani R.A., Ross K., et al. Higher antibody, but not cell-mediated, responses to vaccination in high physically fit elderly. J Appl Physiol 102 3 (2007) 1090-1098
22. Kohut M.L., Cooper M.M., Nickolaus M.S., Russell D.R., and Cunnick J.E. Exercise and psychosocial factors modulate immunity to influenza vaccine in elderly individuals. J Gerontol A: Biol Sci Med Sci 57 9 (2002) M557-M562
23. Smith T.P., Kennedy S.L., and Fleshner M. Influence of age and physical activity on the primary in vivo antibody and T cell-mediated responses in men. J Appl Physiol 97 2 (2004) 491-498
24. Grant R.W., Mariani R.A., Vieira V.J., Fleshner M., Smith T.P., Keylock K.T., et al. Cardiovascular exercise intervention improves the primary antibody response to keyhole limpet hemocyanin (KLH) in previously sedentary older adults. Brain Behav Immun 22 6 (2008) 923-932
25. Kohut M.L., Arntson B.A., Lee W., Rozeboom K., Yoon K.J., Cunnick J.E., et al. Moderate exercise improves antibody response to influenza immunization in older adults. Vaccine 22 17-18 (2004) 2298-2306
26. Schuler P.B., Lloyd L.K., Leblanc P.A., Clapp T.A., Abadie B.R., and Collins R.K. The effect of physical activity and fitness on specific antibody production in college students. J Sports Med Phys Fitness 39 3 (1999) 233-239
27. Whitham M., and Blannin A.K. The effect of exercise training on the kinetics of the antibody response to influenza vaccination. J Sports Sci 21 12 (2003) 991-1000
28. Coleman K.J., and Rager D.R. Effects of voluntary exercise on immune function in rats. Physiol Behav 54 4 (1993) 771-774
29. Jonsdottir I.H., Asea A., Hoffmann P., Dahlgren U.I., Andersson B., Hellstrand K., et al. Voluntary chronic exercise augments in vivo natural immunity in rats. J Appl Physiol 80 5 (1996) 1799-1803
30. Baldwin D.R., Wilcox Z.C., and Zheng G. The effects of voluntary exercise and immobilization on humoral immunity and endocrine responses in rats. Physiol Behav 61 3 (1997) 447-453
31. Elphick G.F., Greenwood B.N., Campisi J., and Fleshner M. Increased serum nIgM in voluntarily physically active rats: a potential role for B-1 cells. J Appl Physiol 94 2 (2003) 660-667
32. Lillard Jr. J.W., Boyaka P.N., Hedrick J.A., Zlotnik A., and McGhee J.R. Lymphotactin acts as an innate mucosal adjuvant. J Immunol 162 4 (1999) 1959-1965
33. Zaharoff D.A., Rogers C.J., Hance K.W., Schlom J., and Greiner J.W. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine 25 11 (2007) 2085-2094
34. Zaharoff D.A., Rogers C.J., Hance K.W., Schlom J., and Greiner J.W. Chitosan solution enhances the immunoadjuvant properties of GM-CSF. Vaccine 25 52 (2007) 8673-8686
35. Fernando P., Bonen A., and Hoffman-Goetz L. Predicting submaximal oxygen consumption during treadmill running in mice. Can J Physiol Pharmacol 71 10/11 (1993) 854-857
36. Dohm M.R., Richardson C.S., and Garland Jr. T. Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. Am J Physiol 267 4 Pt 2 (1994) R1098-R1108
37. Friedman W.A., Garland Jr. T., and Dohm M.R. Individual variation in locomotor behavior and maximal oxygen consumption in mice. Physiol Behav 52 1 (1992) 97-104
38. 2max and running performance in rats. J Appl Physiol 68 1 (1990) 400-403
39. Swallow J.G., Garland Jr. T., Carter P.A., Zhan W.Z., and Sieck G.C. Effects of voluntary activity and genetic selection on aerobic capacity in house mice (Mus domesticus). J Appl Physiol 84 1 (1998) 69-76
40. Rezende E.L., Chappell M.A., Gomes F.R., Malisch J.L., and Garland Jr. T. Maximal metabolic rates during voluntary exercise, forced exercise, and cold exposure in house mice selectively bred for high wheel-running. J Exp Biol 208 Pt 12 (2005) 2447-2458
41. Rodnick K.J., Reaven G.M., Haskell W.L., Sims C.R., and Mondon C.E. Variations in running activity and enzymatic adaptations in voluntary running rats. J Appl Physiol 66 3 (1989) 1250-1257
42. Zhan W.Z., Swallow J.G., Garland Jr. T., Proctor D.N., Carter P.A., and Sieck G.C. Effects of genetic selection and voluntary activity on the medial gastrocnemius muscle in house mice. J Appl Physiol 87 6 (1999) 2326-2333
43. Wisloff U., Najjar S.M., Ellingsen O., Haram P.M., Swoap S., Al-Share Q., et al. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307 5708 (2005) 418-420
44. Davidson S.R., Burnett M., and Hoffman-Goetz L. Training effects in mice after long-term voluntary exercise. Med Sci Sports Exerc 38 2 (2006) 250-255
45. Jequier E. Leptin signaling, adiposity, and energy balance. Ann NY Acad Sci 967 (2002) 379-388
46. Pedersen B.K., and Fischer C.P. Physiological roles of muscle-derived interleukin-6 in response to exercise. Curr Opin Clin Nutr Metab Care 10 3 (2007) 265-271
47. Petersen A.M., and Pedersen B.K. The anti-inflammatory effect of exercise. J Appl Physiol 98 4 (2005) 1154-1162
48. Kohut M.L., Boehm G.W., and Moynihan J.A. Moderate exercise is associated with enhanced antigen-specific cytokine, but not IgM antibody production in aged mice. Mech Ageing Dev 122 11 (2001) 1135-1150
49. Avula C.P., Muthukumar A.R., Zaman K., McCarter R., and Fernandes G. Inhibitory effects of voluntary wheel exercise on apoptosis in splenic lymphocyte subsets of C57BL/6 mice. J Appl Physiol 91 6 (2001) 2546-2552
50. Fu S.C., Qin L., Leung C.K., Chan B.P., and Chan K.M. Regular moderate exercise training prevents decrease of CD4+ T-lymphocytes induced by a single bout of strenuous exercise in mice. Can J Appl Physiol 28 3 (2003) 370-381
51. Davidson S.R., and Hoffman-Goetz L. Freewheel running selectively prevents mouse CD4+ intestinal lymphocyte death produced after a bout of acute strenuous exercise. Brain Behav Immun 20 2 (2006) 139-143
52. Matsuda T., and Hirano T. IL-6. In: Oppenheim J.J., and Feldmann M. (Eds). Cytokine Reference (2000), Academic Press, New York
53. Scheller J., and Rose-John S. Interleukin-6 and its receptor: from bench to bedside. Med Microbiol Immunol 195 4 (2006) 173-183
54. Chen X., Howard O.M., and Oppenheim J.J. Pertussis toxin by inducing IL-6 promotes the generation of IL-17-producing CD4 cells. J Immunol 178 10 (2007) 6123-6129
55. Wan S., Xia C., and Morel L. IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4+ CD25+ T cell regulatory functions. J Immunol 178 1 (2007) 271-279
56. Pasare C., and Medzhitov R. Toll pathway-dependent blockade of CD4+ CD25+ T cell-mediated suppression by dendritic cells. Science 299 5609 (2003) 1033-1036