723
Views
84
CrossRef citations to date
0
Altmetric
Original Article

Cytokine induction during exertional hyperthermia is abolished by core temperature clamping: neuroendocrine regulatory mechanisms

, , , , &
Pages 503-516 | Received 06 Aug 2003, Accepted 02 Feb 2004, Published online: 09 Jul 2009

References

  • Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000; 80: 1055–81.
  • Yang EV, Glaser R. Stress-induced immunomodulation and the implications for health. Int Immunopharmacol 2002; 2: 315–24.
  • Nieman DC. Current perspective on exercise immunology. Curr Sports Med Rep 2003; 2: 239–42.
  • Fallon KE. The acute phase response and exercise: the ultramarathon as prototype exercise. Clin J Sport Med 2001; 11: 38–43.
  • Ostrowski K, Hermann C, Bangash A, Schjerling P, Nielsen JN, Pedersen BK. A trauma-like elevation of plasma cytokines in humans in response to treadmill running. J Physiol (Lond) 1998; 513: 889–94.
  • Shek PN, Shephard RJ. Physical exercise as a human model of limited inflammatory response. Can J Physiol Pharrnacol 1998; 76: 589–97.
  • Rhind SG, Shek PN, Shephard RJ. The impact of exercise on cytokines and receptor expression. Exerc Immunol Rev 1995; 1: 97–148.
  • Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflamma-tory response to exhaustive exercise. Cytokine kinetics. Exerc Irnrnunol Rev 2002; 8: 6–48.
  • Pedersen BK. Exercise and cytokines. Immunology and Cell Biology 2000; 78: 532–5.
  • Brenner I, Shek PN, Zamecnik J, Shephard RJ. Stress hormones and the immunological responses to heat and exercise. Int J Sports Med 1998; 19: 130–43.
  • Hales JRS, Hubbard RW, Gaffin SL. Limitations to heat tolerance. In: Fregly MJ, Blatteis CM, eds, Handbook of Physiology. Oxford: Oxford University Press, 1996; 285–355.
  • Castellani JW, Brenner IKM, Rhind SG. Cold exposure: human immune responses and intracellular cytokine expression. Med Sci Sports Exerc 2002; 34: 2013–20.
  • Shephard RJ, Castellani JW, Shek PN. Immune deficits induced by strenuous exertion under adverse environmental conditions: manifestations and countermeasures. Crit Rev Immunol 1998; 18: 545–68.
  • Brenner IKM, Shek PN, Shephard RJ. Heat exposure and immune function: potential contributions to the immune response. Exerc Irnrnunol Rev 1995; 1: 49–80.
  • Hanson DF. Fever, temperature, and the immune response. Ann NY Acad Sci 1997; 813: 453–64.
  • Pedersen BK, Klokker M, Kappel M. Possible role of hyperthermia and hypoxia in exercise-induced immunomodulation. In: Pedersen BK, ed. Exercise Immunology. Austin, TX: Landes Bioscience, 1997; 61–73.
  • Brenner IK, Castellani JW, Gabaree C, Young Ai, Zamecnik J, Shephard RJ, Shek PN. Immune changes in humans during cold exposure: effects of prior heating and exercise. J Appl Physiol 1999; 87: 699–710.
  • Fairchild KD, Viscardi RM, Hester L, Singh IS, Hasday JD. Effects of hypothermia and hyperthermia on cytokine production by cultured human mononuclear phagocytes from adults and newborns. J Intefer Cytok Res 2000; 20: 1049–55.
  • Jiang Q, Detolla L, Singh IS, Gatdula L, Fitzgerald B, van Rooijen N, Cross AS, Hasday JD. Exposure to febrile temperature upregulates expression of pyrogenic cyto-kines in endotoxin-challenged mice. Am J Physiol 1999; 276: R1653–60.
  • Kappel M, Diamant M, Hansen M, Klokker H, Pedersen BK. Effects of hyperthermia in vitro on proliferative responses of individual blood mononuclear cell subsets, interferon, lymphotoxin, tumor necrosis factor, interleukin 1,2, and 6. Immunology 1991; 73: 304–8.
  • Katschinski DM, Wiedmann GJ, Longo W, d'Oleire FR, Spriggs D, Robins HI. Whole body hyperthermia cytokine induction: a review. Cytokine Growth Factor Rev 1999; 10: 93–7.
  • Mitchell JB, Dugas JP, McFarlin BK, Nelson Mi. Effect of exercise, heat stress, and hydration on immune cell number and function. Med Sci Sports Exerc 2002; 34: 1941–50.
  • Bouchama A, Knochel JP. Heat stroke. N Engl J Med 2002; 346: 1978–88.
  • DuBose DA, Balcius J, Morehouse D. Heat stress and/or endotoxin effects on cytokine expression by human whole blood. Shock 2002; 17: 217–21.
  • Shephard RJ, Shek PN. Immune dysfunction as a factor in heat illness. Crit Rev Irnmunol 1999; 19: 285–302.
  • Shephard RJ. Exercise in the heat: a double threat to the immune system. Phys Sports Med 2002; 29: 21–31.
  • Oberholzer A, Oberholzer C, Moldawer LL. Cytokine signalingregulation of theimmune response in normal and critically ill states. Crit Care Med 2000; 28: N3–12.
  • Elenkov Ii, Chrousos GP. Stress, cytokine patterns and susceptibility to disease. Baillieres Best Pract Res Clin Endocrinol Metab 1999; 13: 583–95.
  • Cross MC, Radomski MW, VanHelder WP, Rhind SG, Shephard RJ. Endurance exercise with and without a thermal clamp: effects on leukocytes and leukocyte subsets. J Appl Physiol 1996; 81: 822–9.
  • Rhind SG, Gannon GA, Shek PN, Brenner IK, Severs Y, Zamecnik J, Buguet A, Natale VM, Shephard RJ, Radomski MW. Contribution of exertional hyperthermia to sympathoadrenal-mediated lymphocyte subset redistribution. J Appl Physiol 1999; 87: 1178–85.
  • Radomski MW, Cross MC, Buguet A. Exercise-induced hyperthermia and hormonal responses to exercise. Can J Physiol Pharmacol 1998; 76: 547–52.
  • DeRijk R, Michelson D, Karp B, Petrides J, Galliven E, Deuster P, Paciotti G, Gold PW, Sternberg EM. Exercise and circadian rhythm-induced variations in plasma cortisol differentially regulate interleukin-1 beta (IL-1 beta), IL-6, and tumor necrosis factor-alpha (TNF alpha) production in humans: high sensitivity of TNF alpha and resistance of IL-6. J Clin Endocrinol Metab 1997; 82: 2182–91.
  • Rhind SG, Castellani JW, Brenner IK, Shephard RJ, Zamecnik J, Montain Si, Young Ai, Shek PN. Intracellular monocyte and serum cytokine expression is modulated by exhaust-ing exercise and cold exposure. Am J Physiol 2001; 281: R66–75.
  • Sondergaard SR, Ostrowski K, Ullum H, Pedersen BK. Changes in plasma concentra-tions of interleukin-6 and interleukin-1 receptor antagonists in response to adrenaline infusion in humans. Eur J Appl Physiol 2000; 83: 95–8.
  • Gannon GA, Rhind SG, Suzui M, Shek PN, Shephard RJ. Circulating levels of peripheral blood leucocytes and cytokines following competitive cycling. Can J Appl Physiol 1997; 22: 133–47.
  • Nehlsen-Cannarella SL, Fagoaga OR, Nieman DC, Henson DA, Butterworth DE, Schmitt RL, Bailey EM, Warren BJ, Utter A, Davis JM. Carbohydrate and the cytokine response to 2.5 h of running. J Appl Physiol 1997; 82: 1662–7.
  • Papanicolaou DA, Petrides JS, Tsigos C, Bina S, Kalogeras KT, Wilder R, Gold PW, Deuster PA, Chrousos GP. Exercise stimulates interleukin-6 secretion: inhibition by glucocorticoids and correlation with catecholamines. Am J Physiol 1996; 271: E601–5.
  • Ullum H, Haahr PM, Diamant M, Palmo J, Halkjxr-Kristensen J, Pedersen BK. Bicycle exercise enhances plasma IL-6 but does not change IL-1 alpha, IL-1 beta, IL-6, or TNF-alpha pre-mRNA in BMNC. J Appl Physiol 1994; 77: 93–7.
  • Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol (Lond) 1999; 515: 287–91.
  • Toft AD, Thorn M, Ostrowski K, Asp S, Moller K, Iversen S, Hermann C, Sondergaard SR, Pedersen BK. N-3 polyunsaturated fatty acids do not affect cytokine response to strenuous exercise. J Appl Physiol 2000; 89: 2401–6.
  • Rhind SG, Gannon GA, Shephard RJ, Shek PN. Indomethacin modulates circulating cytokine responses to strenuous exercise in humans. Cytokine 2002; 19: 153–8.
  • Akimoto T, Akama T, Tatsuno M, Saito M, Kono I. Effect of brief maximal exercise on circulating levels of interleukin-12. Eur J Appl Physiol 2000; 81: 510–2.
  • Zellner M, Hergovics N, Roth E, Jilma B, Spittler A, Oehler R. Human monocyte stimulation by experimental whole body hyperthermia. Wien Klin Wochenschr 2002; 114: 102–7.
  • Ostberg JR, Taylor SL, Baumann H, Repasky EA. Regulatory effects of fever-range whole-body hyperthermia on the LPS-induced acute inflammatory response. J Leuk Biol 2000; 68: 815–20.
  • Febbraio MA, Starkie RL, Rhind SG, Shek PN. The cellular origin of plasma cytokine expression after acute exercise. Am J Physiol Regul Integr Comp Physiol 2002; 282: R1253-7; author reply R54–7.
  • Shephard RJ. Cytokine responses to physical activity, with particular reference to IL-6: sources, actions, and clinical implications. Crit Rev Irnmunol 2002; 22: 165–82.
  • Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. Faseb J 2002; 16: 1335–47.
  • Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JH, Senden J, Saris WH, Wagenmakers AI Relationship between gastro-intestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci 2000; 98: 47–55.
  • Smith LL. Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress? Med Sci Sports Exerc 2000; 32: 317–31.
  • Marshall JC. The gut as a potential trigger of exercise-induced inflammatory responses. Can J Physiol Pharrnacol 1998; 76: 479–84.
  • Liao W, Rudling M, Angelin B. Growth hormone potentiates the in vivo biological activities of endotoxin in the rat. Eur J Clin Invest 1996; 26: 254–8.
  • Russell JA. Catecholamines and the splanchnic circulation. Crit Care Med 1999; 27: 242–3.
  • Howlett TA. Hormonal responses to exercise and training: a short review. Clin Endocrinol (Oxf) 1987; 26: 723–42.
  • Kappel M, Gyhrs A, Galbo H, Pedersen BK. The response on glucoregulatory hormones of in vivo whole body hyperthermia. Int J Hypertherrnia 1997; 13: 413–21.
  • Buckler JMH. The relationship between changes in plasma growth hormone levels and body temperature occurring with exercise in man. Biomedicine 1973; 19: 193–7.
  • Weigent DA, Blalock JE. Bidirectional communication between the immune and neuro-endocrine systems. In: Plotnikoff NP, Faith RE, Murgo AJ, Good RA, eds, Cytokines: Stress and Immunity. Boca Raton: CRC Press, 1999; 173–86.
  • Wilckens T, De Rijk R. Glucocorticoids and immune function: unknown dimensions and new frontiers. Irnrnunol Today 1997; 18: 418–24.
  • Bozzola M, De Amici M, Zecca M, Schimpff RM, Rapaport R. Modulating effect of human growth hormone on tumour necrosis factor-alpha and interleukin-lbeta. Eur J Endocrinol 1998; 138: 640–3.
  • Kappel M, Hansen MB, Diamant M, Pedersen BK. In vitro effects of human growth hormone on the proliferative responses and cytokine production of blood mononuclear cells. Horrn Metab Res 1994; 26: 612–4.
  • Weigent DA. Immunoregulatory properties of growth hormone and prolactin. Pharrncol Therap 1996; 69: 237–57.
  • Zarkesh-Esfahani SH, Kolstad O, Metcalfe RA, Watson PF, von Laue S, Walters S, Revhaug A, Weetman AP, Ross RJ. High-dose growth hormone does not affect pro-inflammatory cytokine (tumor necrosis factor-alpha, interleukin-6, and interferon-gamma) release from activated peripheral blood mononuclear cells or after minimal to moderate surgical stress. J Clin Endocrinol Metab 2000; 85: 3383–90.
  • Uronen-Hansson, Allen ML, Lichtarowicz KE, Aynsley-Green A, Cole TJ, Hoiden-Guthenberg I, Fryklund L, Klein N. Growth hormone enhances proinflammatory cytokine production by monocytes in whole blood. Growth Hormone IGF Res 2003; 13: 282–6.
  • Brattsand R, Linden M. Cytokine modulation by glucocorticoids: mechanisms and actions in cellular studies. Aliment Pharrnacol Ther 1996; 10: 81–90.
  • Tilg H, Dinarello CA, Mier JW. IL-6 and acute-phase proteins: anti-inflammatory and immunosuppressive mediators. Irnrnunol Today 1997; 18: 428–32.
  • Hershko DD, Robb BW, Luo G, Paxton JR, Hasselgren PO. Interleukin-6 induces thermotolerance in cultured Caco-2 cells independent of the heat shock response. Cytokine 2003; 21: 1–9.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.