SciELO - Scientific Electronic Library Online

SciELO - Scientific Electronic Library Online

Article References

TERRA, Rodrigo; SILVA, Sílvia Amaral Gonçalves da; PINTO, Verônica Salerno  and  DUTRA, Patrícia Maria Lourenço. Efeito do exercício no sistema imune: resposta, adaptação e sinalização celular. Rev Bras Med Esporte [online]. 2012, vol.18, n.3, pp.208-214. ISSN 1517-8692.

    1. Handschin C, Spiegelman BM. The role of exercise and PGC1α in inflammation and chronic disease. Nature 2008;454:463-9. [ Links ]

    2. Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: Regulation integration and adaption. Physiol Reviews 2000;80:1055-81. [ Links ]

    3. Rosa LF, Vaisberg MW. Influências do exercício na reposta imune. Rev Bras Med Esporte 2002;8:167-72. [ Links ]

    4. Leandro CG, Castro RM, Nascimento E, Pithon-Curi TC, Curi R. Mecanismos adaptativos do sistema imunológico em resposta ao treinamento físico. Rev Bras Med Esporte 2007;13:343-48. [ Links ]

    5. Pollock ML, Gaesser GA, Butcher JD, Després J-P, Dishman RK, Franklin BA, et al. ACSM Position Stand: The Recommended Quantity And Quality Of Exercise For Developing And Maintaining Cardiorespiratory And Muscular Fitness, And Flexibility In Healthy Adults. Med Sci Sports Exerc 1998;30:975-91. [ Links ]

    6. Haskell WL, Lee I-M, Pate RR, Powell KE, Blair SN, Franklin BA, et al. Physical Activity and Public Health: Updated Recommendation for Adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 2007;39:1423-34. [ Links ]

    7. Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, Shephard RJ, et al. Position Statement Part two: Maintaining immune health. Exerc Immunol Rev 2011;17:64-103. [ Links ]

    8. Romagnani S. Type 1 T helper and type 2 T helper cells: functions, regulation and role in protection and disease. Int J Clin Lab Res 1991;21:152-8. [ Links ]

    9. Del Prete G. The complexity of the CD4 T-cell responses: old and new T-cell subsets. Parassitologia 2008;50:9-16. [ Links ]

    10. Moretta A, Marcenaro E, Parolini S, Ferlazzo G, Moretta L. NK cells at the interface between innate and adaptive immunity. Cell Death Differ 2008;15:226-33. [ Links ]

    11. Dinarello CA, Mier JW. Interleukins Annu Rev Med 1986;37:173-8. [ Links ]

    12. Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombes JS. Plasma cytokine changes in relation to exercise intensity and muscle damage. Eur J Appl Physiol 2005;95:514-21. [ Links ]

    13. Vilcek J, Feldman M. Historical review: cytokines as therapeutic and targets of therapeutics. Trends Pharmacol Sci 2004;25:201. [ Links ]

    14. Elenkov IJ, Chrousos GP, Wilder RL. Neuroendocrine regulation of IL-12 and TNF-alpha/IL-10 balance. Clinical implications. Ann NY Acad Sci 2000;917:94-105. [ Links ]

    15. Cannon JG. Infammatory cytokines in nonpathological states. News Physiol Sci 2000;15:298-303. [ Links ]

    16. Heinzel F, Hujer A, Ahmed F, Rerko R. In vivo production and function of IL-12p40 homodimers. J Immunol 1997;158:4381-8. [ Links ]

    17. Omata N, Yasutomi M, Yamada A, Iwasaki H, Mayumi M, Ohshima Y. Monocyte chemoattractant protein-1 selectively inhibits the acquisition of CD40 ligand-dependent IL-12-producing capacity of monocyte-derived dendritic cells and modulates Th1 immune response. J Immunol 2002;169:4861-6. [ Links ]

    18. Elenkov IJ, Papanicolaou DA, Wilder RL, Chrousos GP. Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians 1996;108:374-81. [ Links ]

    19. Ramirez F, Fowell DJ, Puklavec M, Simmonds S, Mason D. Glucocorticoids promote a Th2 cytokine response by CD4+ T cells in vitro. J Immunol 1996;156:2406-12. [ Links ]

    20. Blotta MH, DeKruy RH, Umetsu DT. Corticosteroids inhibit IL-12 production in human monocytes and enhance their capacity to induce IL-4 synthesis in CD4+ lymphocytes. J Immunol 1997;158:5589-95. [ Links ]

    21. Agarwal SK, Marshall GD. Beta-adrenergic modulation of human type-1/type-2 cytokine balance. J Allergy Clin Immunol 2000;105:91-8. [ Links ]

    22. Demeure CE, Yang LP, Desjardins C, Raynauld P, Delespesse G. Prostaglandin E2 primes naive T cells for the production of anti-inflammatory cytokines. Eur J Immunol 1997;27:3526-31. [ Links ]

    23. Kalinski P, Vieira PL, Schuitemaker JH, De Jong EC, Kapsenberg ML. Prostaglandin E2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001;97:3466-9. [ Links ]

    24. Sondergaard SR, Ostrowski K, Ullum H, Pedersen BK. Changes in plasma concentrations of interleukin-6 and interleukin-1 receptor antagonists in response to adrenaline infusion in humans. Eur J Appl Physiol 2000;83:95-8. [ Links ]

    25. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol 2003;285:E433-7. [ Links ]

    26. Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation integration and adaption. Physiol Rev 2000;80:1055-81. [ Links ]

    27. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 1999;515:287-91. [ Links ]

    28. Pedersen BK, Febbraio MA. Muscle as an Endocrine Organ: Focus on Muscle-Derived Interleukin-6. Physiol Rev 2008;88:1379-406. [ Links ]

    29. Pedersen BK, Steensberg A, Schjerling P. Muscle derived interleukin-6: possible biological effects. J Physiol 2001;536:329-37. [ Links ]

    30. Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 2002;16:1335-47. [ Links ]

    31. Pedersen BK, Steensberg A, Fischer C, Keller C, Keller P, Plomgaard P, et al. Searching for the exercise factor – is IL-6 a candidate? J Mus Res Cell Motil 2003;24:113-9. [ Links ]

    32. Febbraio MA, Pedersen BK. Contraction-induced myokine production and release: is skeletal muscle an endocrine organ? Exerc Sport Sci Rev 2005;33:114-9. [ Links ]

    33. Pedersen BK, Fischer CP. Physiological roles of muscle-derived interleukin-6 in response to exercise. Curr Opin Clin Nutr Metab Care 2007;10:265-71. [ Links ]

    34. Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund PB. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 2000;529:237-42. [ Links ]

    35. Fischer CP, Hiscock N, Basu S, Vessby B, Kallner A, Sjoberg LB, et al. Supplementation with vitamins C and E inhibits the release of interleukin-6 from contracting human skeletal muscle. J Physiol 2004;558:633-45. [ Links ]

    36. Nielsen S, Pedersen BK. Skeletal muscle as an immunogenic organ. Curr Opin Pharmacol 2008;8:346-51. [ Links ]

    37. Pedersen, B.K. Muscles and their myokines. J Exp Biol 2011;214:337-46. [ Links ]

    38. Gavriele, Ashlagi-Amiri RT, Eliakim A, Nemet D, Zigel L, Berger-Achituv S, et al. The Effect of Aerobic Exercise on Neutrophil Functions. Med Sci Sports Exerc 2008;40:1623-8. [ Links ]

    39. Butterfield TA, Best TM, Merrick MA. The Dual Roles of Neutrophils and Macrophages in Inflammation: A Critical Balance Between Tissue Damage and Repair. J Athle Training 2006;41:457-65. [ Links ]

    40. Brickson S, Hollander J, Corr DT, Ji LL, Best TM. Oxidant production and immune response after stretch injury in skeletal muscle. Med Sci Sports Exerc 2001;33:2010-5. [ Links ]

    41. Wolach B, Falk B, Gavrieli R, Kodesh E, Eliakim A. Neutrophil function response to aerobic and anaerobic exercise in female judoka and untrained subjects. Br J Sports Med 2000;34:23-7. [ Links ]

    42. Wolach B, Gavrieli R, Ben-Dror SG, Zigel L, Eliakim A, Falk B. Transient decrease of neutrophil chemotaxis following aerobic exercise. Med Sci Sports Exerc 2005;37:949-54. [ Links ]

    43. Walsh, N. Effect of oral glutamine supplementation on human neutrophil lipopolysaccharide-stimulated degranulation following prolonged exercise. Int J Sport Nutr Exerc Metab 2000 ;10 :39-50. [ Links ]

    44. Morozov VI, et al. The effects of high-intensity exercise on skeletal muscle neutrophil myeloperoxidase in untrained and trained rats. Eur J Appl Physiol 2006;97:716-22. [ Links ]

    45. Gleeson M, McFarlin B, Flynn, M. Exercise and Toll-like receptors. Exerc Immunol Rev 2006;12:34-5. [ Links ]

    46. Kizaki T, Takemasa T, Sakurai T, Izawa T, Hanawa T, Kamiya T, et al. Adaptation of macrophages to exercise training improves innate immunity. Biochem Biophys Res Communic 2008;372:152-6. [ Links ]

    47. Jost J, Weiss M, Weicker R. Sympathoadrenergic regulation and the adrenoceptor system. J Appl Physiol 1990;68:897-904. [ Links ]

    48. Kohm AP, Sanders VM. Norepinephrine: a messenger from the brain to the immune system. Immunol Today 2000;21:539-42. [ Links ]

    49. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000;18:767-811. [ Links ]

    50. Chiang LM, Chen YJ, Chiang J, Lai LY, Chen YY, Liao HF. Modulation of Dendritic Cells by Endurance Training. Int J Sports Med 2007;28:798-803. [ Links ]

    51. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer cell subsets. Trends Immunol 2001;22:633-40. [ Links ]

    52. Poli A, Michel T, Thérésine M, Andrès E, Hentges F, Zimmer J. CD56bright natural killer (NK) cells: an important NK cell subset. Immunology 2009;126:458-65. [ Links ]

    53. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol 1986;136:4480-6. [ Links ]

    54. Caligiuri MA. Human natural killer cells. Blood 2008;112:461-9. [ Links ]

    55. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003;101:3052-7. [ Links ]

    56. Mocikat R, Braumuller H, Gumy A, Egeter O, Ziegler H, Reusch U, et al. Natural killer cells activated by MHC class I (low) targets prime dendritic cells to induce protective CD8 T cell responses. Immun 2003;19:561-9. [ Links ]

    57. Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII- positive and negative natural killer cells. J Immunol 1989;143:3183-91. [ Links ]

    58. Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, Carson WE, Caligiuri MA. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 2001;97:3146-51. [ Links ]

    59. Timmons BW, Cieslak T. Human Natural Killer Cell Subsets and Acute Exercise: A Brief Review. Exerc Immunol Rev 2008;14:8-23. [ Links ]

    60. Nagao F, Suzui M, Takeda K, Yagita H, Okumura K. Mobilization of NK cells by exercise: downmodulation of adhesion molecules on NK cells by catecholamines. Am J Physiol Regul Integr Comp Physiol 2000;279:R1251-6. [ Links ]

    61. Dela F, Mikines KJ, Von Linstow M, Galbo H. Heart rate and plasma catecholamines during 24 h of everyday life in trained and untrained men. J Appl Physiol 1992;73:2389-95. [ Links ]

    62. Gannon GA, Rhind SG, Suzui M, Shek PN, Shephard RJ. Circulationg levels of peripheral blood leukocytes and cytokines following competitive cycling. Can J Appl Physiol 1997;22:133-47. [ Links ]

    63. Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom P, Lundberg IE, et al. Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol 2004;556:983-1000. [ Links ]

    64. Timmons BW, Tarnopolsky MA, Bar-Or O. Sex-based effects on the distribution of NK cell subsets in response to exercise and carbohydrate intake in adolescents. J Appl Physiol 2006;100:1513-9. [ Links ]

    65. 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;38:864-74. [ Links ]

    66. Timmons BW, Bar-Or O. Evidence of sex-based differences in natural killer cell responses to exercise and carbohydrate intake in children. Eur J Appl Physiol 2007;101:233-40. [ Links ]

    67. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J 2005;19:1498-500. [ Links ]

    68. Dalbeth N, Gundle R, Davies RJ, Lee YC, McMichael AJ, Callan MF. CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J Immunol 2004;173:6418-26. [ Links ]

    69. Lash GE, Schiessl B, Kirkley M, Innes BA, Cooper A, Searle RF et al. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J Leukoc Biol 2006;80:572-80. [ Links ]

    70. Oshida Y, Yamanouchi K, Hayamizu S, Sato Y. Effect of acute physical exercise on lymphocyte subpopulations in trained and untrained subjects. Int J Sports Med 1988;9:137-40. [ Links ]

    71. Hansen JB, Wilsgard L, Osterud B. Biphasic changes in leukocytes induced by strenuous exercise. Eur J Appl Physiol 1991;62:157-61. [ Links ]

    72. Navalta, JW, Sedlock DA, Park KS. Effect of Exercise Intensity on Exercise-Induced Lymphocyte Apoptosis. Int J Sports Med 2007;28:539-42. [ Links ]

    73. Hsu T-G, Hsu K-M, Kong C-W, Lu F-J, Cheng H, Tsai K. Leukocyte mitochondria alterations after aerobic exercise in trained human subjects. Med Sci Sports Exerc 2002;34:438-42. [ Links ]

    74. Steensberg A, Morrow J, Toft AD, Bruunsgaard H, Pedersen BK. Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur J Appl Physiol 2002;87:38-42. [ Links ]

    75. Jong-Shyan Wang & Yu-Hsiang Huang. Effects of exercise intensity on lymphocyte apoptosis induced by oxidative stress in men. Eur J Appl Physiol 2005;95:290-7. [ Links ]

    76. Levada-Pires AC, Cury-Boaventura MF, Gorjao R, Hirabara SM, Puggina EF, Peres CM, et al. Neutrophil Death Induced by a Triathlon Competition in Elite Athletes. Med Sci Sports Exerc 2008;40:1447-54. [ Links ]

    77. Kruger K, Lechtermann A, Fobker M, Volker K, Mooren, FC. Exercise-induced redistribution of T lymphocytes is regulated by adrenergic mechanisms. Brain Behave Immun 2008;22:324-38. [ Links ]

    78. Jenkins MK, Taylor PS, Norton SD, Urdahl KB. CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J Immunol 1991;147:2461-6. [ Links ]

    79. Cerdan C, Martin Y, Courcoul M, Brailly H, Mawas C, Birg F, et al. Prolonged IL-2 receptor á/CD25 expression after T cell activation via the adhesion molecules CD2 and CD28. Demonstration of combined transcriptional and posttranscriptional regulation. J Immunol 1992;149:2255-61. [ Links ]

    80. Utsuyama M, Hirokawa K, Kurashima C, Fukayama M, Inamatsu T, Suzuki K et al. Differential age-change in the numbers of CD4+CD45RA+ and CD4+CD29+ T cell subsets in human peripheral blood. Mech Ageing Dev 1992;63:57-68. [ Links ]

    81. Shimizu K, Kimura F, Akimoto T, Akama T, Tanabe K, Nishijima, et al. Effect of moderate exercise training on T-helper cell subpopulations in elderly people. Exerc Immunol Rew 2008;14:24-37. [ Links ]

    82. Koizumi K, Kimura F, Akimoto T, Akama T, Kumai Y, Tanaka H, et al. Effects of long-term exercise training on peripheral lymphocyte subsets in elderly subjects. Jpn J Phys Fitness Sports Med 2003;52:193-202. [ Links ]

    83. Kohut ML, Senchina, DS. Reversing age-associated immunosenescence via exercise. Exerc Immunol Rev 2004;10:6-41. [ Links ]

    84. Cannon JG, Kluger MJ. Endogenous pyrogen activity in human plasma after exercise. Sci 1983;220:617-9. [ Links ]

    85. Northoff H, Berg A. Immunologic mediators as parameters of the reaction to strenuous exercise. Int J Sports Med 1991;12:9-15. [ Links ]

    86. Barra NG, Reid S, MacKenzie R, Werstuck G, Trigatti BL, Richards C, Holloway AC, Ashkar AA. Interleukin-15 contributes to the regulation of murine adipose tissue and human adipocytes. Obesity (Silver Springs) 2010;18:1601-7. [ Links ]

    87. Wunderlich FT, Strohle P, Konner AC, Gruber S, Tovar S, Bronneke HS, et al. Interleukin-6 signaling in liver-parenchymal cells suppresses hepatic inflammation and improves systemic insulin action. Cell Metab 2010;12:237-49. [ Links ]

    88. Inoue S, Unsinger J, Davis CG, Muenzer JT, Ferguson TA, Chang K, et al. IL-15 prevents apoptosis, reverses innate and adaptive immune dysfunction, and improves survival in sepsis. J Immunol 2010;184:1401-9. [ Links ]

    89. Tamura Y, Watanabe K, Kantani T, Hayashi J, Ishida N, Kaneki M. Upregulation of circulating IL-15 by treadmill running in healthy individuals: Is IL 15 an endocrine mediator of the beneficial effects of endurance exercise? Endocr J 2011;58:211-5. [ Links ]

    90. Suzuki K, Nakaji S, Kurakake S, Totsuka M, Sato K, Kuriyama T, et al. Exhaustive exercise and type-1/type-2 cytokine balance with special focus on interleukin-12 p40/p70. Exerc Immunol Rev 2003;9:48-57. [ Links ]

    91. Hirose L, Nosaka K, Newton M, Laveder A, Kano M, Peake JM, et al. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev 2004;10:75-90. [ Links ]

    92. Nieman DC, Davis JM, Brown VA, Henson DA, Dumke CL, Utter AC, et al. Influence of carbohydrate ingestion on immune changes after 2 h of intensive resistance training. J Appl Physiol 2004;96:1292-8. [ Links ]

    93. Toft AD, Jensen LB, Bruunsgaard H, Ibfelt T, Halkjaer-Kristensen J, Febbraio M, et al. Cytokine response to eccentric exercise in young and elderly humans. Am J Physiol 2002;283:C289-95. [ Links ]

    94. Petersen AM, Pedersen BK. The anti-infammatory effect of exercise. J Appl Physiol 2005;98:1154-62. [ Links ]

    95. Drenth JP, Krebbers RJ, Bijzet J, van der Meer JW. Increased circulating cytokine receptors and ex vivo interleukin-1 receptor antagonist and interleukin1b production but decreased tumour necrosis factor-a production after a 5-km run. Eur J Clin Invest 1998;28:866-72. [ Links ]

    96. Moldoveanu AI, Shephard RJ, Shek PN. Exercise elevates plasma levels but not gene expression of IL-1b, IL-6, and TNF-α in blood mononuclear cells. J Appl Physiol 2000;89:1499-504. [ Links ]

    97. Keller C, Keller P, Giralt M, Hidalgo J, Pedersen BK. Exercise normalises overexpression of TNF-α in knockout mice. Biochem. Biophys Res Commun 2004;321:179-82. [ Links ]

    98. Bruunsgaard H. Physical activity and modulation of systemic low-level inflammation. J Leuk Biol 2005;78:819-35. [ Links ]

    99. Flynn M, McFarlin BK, Markofski MA. The anti-inflammatory actions of exercise training. Am J Lifestyle Med 2007;1:220-35. [ Links ]

    100. Janeway CA, Travers P, Walport M, Capra J. Imunobiologia: O sistema imune na saúde e na doença – 6 ed. 2007; Editora Artmed. [ Links ]

    101. Peter C. Heinrich, Iris Behrmann, Serge Haan, Heike M. Hermanns, Gerhard Muller-Newen & Fred Schaper. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003;374:1-20. [ Links ]

    102. Robson-Ansley P, Cockburn E, Walshe I, Stevenson E, Nimmo M. The effect of exercise on plasma soluble IL-6 receptor concentration: a dichotomous response. Exerc Immunol Rev 2010;16:56-76. [ Links ]

    103. Wullschleger S, et al. TOR signaling in growth and metabolism. Cell 2006;124:471-84. [ Links ]

    104. Yang Q, Guan KL. Expanding mTOR signaling. Cell Res 2007;17:666-81. [ Links ]

    105. Thomson AW, Turnquist HR, Raimondi G. Immunoregulatory functions of mTOR inhibition. Nat Immunol Rev 2009;324-37. [ Links ]

    106. Weichhart T, et al. The TSC–mTOR signaling pathway regulates the innate inflammatory response. Immun 2008;29:565-77. [ Links ]

    107. Atherton PJ, Babraj JA, Smith K, Singh J, Rennie MJ, Wackerhage H. Selective activation of AMPK-PGC-1α or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 2005;1-23. [ Links ]