Changes in spontaneous and lps-induced ex vivo cytokine production and mrna expression in male and female athletes following prolonged exhaustive exercise

Exercise Immunology Review

Volumn 19, Issue , 2013, Pages 8-28

  Abbasi, Asghar ^a,b   Fehrenbach, Elvira ^a   Hauth, Melanie ^a   Walter, Michael ^a   Hudemann, Jens ^a   Wank, Veit ^b   Niess, Andreas M ^a   Northoff, Hinnak ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cytokine; Endotoxin; Ex vivo; Lipopolysaccharide; Menstrual cycle; Sex differences

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ARTICLE; ATHLETE; BLOOD CULTURE; CYTOKINE PRODUCTION; DOWN REGULATION; EX VIVO STUDY; EXERCISE; GENE EXPRESSION; MONOCYTE; PROTEIN EXPRESSION; SEX DIFFERENCE; ADULT; BIOSYNTHESIS; FEMALE; HUMAN; IMMUNOLOGY; MALE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ADULT; ATHLETES; CYTOKINES; EXERCISE; FEMALE; HUMANS; LIPOPOLYSACCHARIDES; MALE; PHYSICAL EXERTION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84884172450     PISSN: 10775552     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Angstwurm MW, Gartner R, Ziegler-Heitbrock HWL: Cyclic plasma IL-6 levels during normal menstrual cycle. Cytokine 1997; 9: 370-374.
2. Bellone G, ste-Amezaga M, Trinchieri G, et al. Regulation of NK cell functions by TGF-beta 1. J Immunol. 1995;155:1066-73.
3. Beutler B. Endotoxin, toll-like receptor 4, and the afferent limb of innate immunity. Curr Opin Microbiol. 2000;3:23-8.
4. Bouman A, Moes H, Heineman MJ, de Leij LFMH, Faas MM: The immune response during the luteal phase of the ovarian cycle: increasing sensitivity of human monocytes to endotoxin. Fertil Steril. 2001; 76: 555-559.
5. Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J. The serum levels of growth factors: PDGF, TGF-beta and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol. 2006;57:189-97.
6. Davis JM, Kohut ML, Colbert LH, et al. Exercise, alveolar macrophage function, and susceptibility to respiratory infection. J Appl Physiol. 1997;83:1461-6.
7. Degerstrøm J ØB. Increased inflammatory response of blood cells to repeated bout of endurance exercise. Med Sci Sports Exerc. 2006;38:1297-303.
8. Dickhuth HH, Huonker M, Münzel T, Drexler H, Berg A, Keul J. Individual anaerobic threshold for evaluation of competitive athletes and patients with left ventricular dysfunction. In: Advances in Ergometry, edited by N.Bachl TEGHLe. Berlin: Springer, 1991, p. 73-79.
9. Drenth JP, Krebbers RJ, Bijzet J, et al. Increased circulating cytokine receptors and ex vivo interleukin-1 receptor antagonist and interleukin-1beta production but decreased tumour necrosis factor-alpha production after a 5-km run. Eur J Clin Invest. 1998;28:866-72.
10. Drenth JP, Van Uum SH, Van DM, et al. Endurance run increases circulating IL-6 and IL-1ra but downregulates ex vivo TNF-alpha and IL-1 beta production. J Appl Physiol. 1995;79:1497-503.
11. Garcia JJ, Bote E, Hinchado MD, et al.A single session of intense exercise improves the inflammatory response in healthy sedentary women. J Physiol Biochem. 2011;67:87-94.
12. Gavin TP, Spector DA, Wagner H, et al. Effect of captopril on skeletal muscle angiogenic growth factor responses to exercise. J Appl Physiol. 2000;88:1690-7.
13. Heinemeier K, Langberg H, Kjaer M. Exercise-induced changes in circulating levels of transforming growth factor-beta-1 in humans: methodological considerations. Eur J Appl Physiol. 2003;90:171-7.
14. Furusawa K, Tajima F, TanakaY, Ide M and Ogata H. Short-term attenuation of natural killer cell cytotoxic activity in wheelchair marathoners with paraplegia. Arch.Phys.Med.Rehabil. 79: 1116-1121, 1998.
15. Furusawa K, Tajima F, UmezuY, Ueta M, Ide M, Mizushima T and Ogata H. Activation of natural killer cell function in recreational athletes with paraplegia during a wheelchair half-marathon race. Arch.Phys.Med.Rehabil. 84: 706-711, 2003.
16. Garshick E, Stolzmann KL, Gagnon DR, Morse LR and Brown R. Systemic inflammation and reduced pulmonary function in chronic spinal cord injury. PM R. 3: 433-439, 2011.
17. Garstang SV and Miller-Smith SA. Autonomic nervous system dysfunction after spinal cord injury. Phys.Med.Rehabil.Clin.N.Am. 18: 275-96, vi-vii, 2007.
18. Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS and Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat.Rev.Immunol. 11: 607-615, 2011.
19. Gold JR and Gold MM. Access for all: The rise of the Paralympic Games. J.R.Soc.Promot.Health. 127: 133-141, 2007.
20. Goosey-Tolfrey V. Physiological profiles of elite wheelchair basketball players in preparation for the 2000 Paralympic Games. Adapt.Phys.Activ Q. 22: 57-66, 2005.
21. Goosey-Tolfrey VL, Foden E, Perret C and Degens H. Effects of inspiratory muscle training on respiratory function and repetitive sprint performance in wheelchair basketball players. Br.J.Sports Med. 44: 665-668, 2010.
22. Guerrero AR, Uchida K, Nakajima H, Watanabe S, Nakamura M, Johnson WE and Baba H. Blockade of interleukin-6 signaling inhibits the classic pathway and promotes an alternative pathway of macrophage activation after spinal cord injury in mice. J.Neuroinflammation 9: 40, 2012.
23. Held KS, Steward O, Blanc C and Lane TE. Impaired immune responses following spinal cord injury lead to reduced ability to control viral infection. Exp.Neurol. 226: 242-253, 2010.
24. Hettinga FJ, Valent L, Groen W, van Drongelen S, de Groot S and van der Woude LH. Hand-cycling: An active form of wheeled mobility, recreation, and sports. Phys.Med.Rehabil.Clin.N.Am. 21: 127-140, 2010.
25. Huang TS, Wang YH, Lee SH and Lai JS. Impaired hypothalamus-pituitary- adrenal axis in men with spinal cord injuries. Am.J.Phys.Med.Rehabil. 77: 108-112, 1998.
26. Hullemann KD, List M, Matthes D, Wiese G and Zika D. Spiroergometric and telemetric investigations during the XXI International Stoke Mandeville Games 1972 in Heidelberg. Paraplegia 13: 109-123, 1975.
27. Ibarra A, Jimenez A, Cortes C and Correa D. Influence of the intensity, level and phase of spinal cord injury on the proliferation of T cells and T-cell-dependent antibody reactions in rats. Spinal Cord 45: 380-386, 2007.
28. Iversen PO, Hjeltnes N, Holm B, Flatebo T, Strom-Gundersen I, Ronning W, Stanghelle J and Benestad HB. Depressed immunity and impaired proliferation of hematopoietic progenitor cells in patients with complete spinal cord injury. Blood 96: 2081-2083, 2000.
29. Jonsdottir IH. Special feature for the Olympics: effects of exercise on the immune system: neuropeptides and their interaction with exercise and immune function. Immunol.Cell Biol. 78: 562-570, 2000.
30. Kappel M, Tvede N, Galbo H, Haahr PM, Kjaer M, Linstow M, Klarlund K and Pedersen BK. Evidence that the effect of physical exercise on NK cell activity is mediated by epinephrine. J.Appl.Physiol. 70: 2530-2534, 1991.
31. Kawashima N, Nakazawa K, Ishii N, Akai M and Yano H. Potential impact of orthotic gait exercise on natural killer cell activities in thoracic level of spinal cord-injured patients. Spinal Cord 42: 420-424, 2004.
32. Keller SE, Weiss JM, Schleifer SJ, Miller NE and Stein M. Stress-induced suppression of immunity in adrenalectomized rats. Science 221: 1301-1304, 1983.
33. Kjaer M, Secher NH, Bangsbo J, Perko G, Horn A, Mohr T and Galbo H. Hormonal and metabolic responses to electrically induced cycling during epidural anesthesia in humans. J.Appl.Physiol. 80: 2156-2162, 1996.
34. Kliesch WF, Cruse JM, Lewis RE, Bishop GR, Brackin B and Lampton JA. Restoration of depressed immune function in spinal cord injury patients receiving rehabilitation therapy. Paraplegia 34: 82-90, 1996.
35. Klokker M, Mohr T, Kjaer M, Galbo H and Pedersen BK. The natural killer cell response to exercise in spinal cord injured individuals. Eur.J.Appl.Physiol.Occup.Physiol. 79: 106-109, 1998.
36. Kouda K, Furusawa K, Sugiyama H, Sumiya T, Ito T, Tajima F and Shimizu K. Does 20-min arm crank ergometer exercise increase plasma interleukin-6 in individuals with cervical spinal cord injury? Eur.J.Appl.Physiol. 112: 597-604, 2011.
37. Krassioukov A. Autonomic function following cervical spinal cord injury. Respir.Physiol.Neurobiol. 169: 157-164, 2009.
38. Landmann RM, Muller FB, Perini C, Wesp M, Erne P and Buhler FR. Changes of immunoregulatory cells induced by psychological and physical stress: relationship to plasma catecholamines. Clin.Exp.Immunol. 58: 127-135, 1984.
39. Leicht CA, Bishop NC and Goosey-Tolfrey VL. Mucosal immune responses during court training in elite tetraplegic athletes. Spinal Cord 50: 760-765, 2012.
40. Leicht CA, Bishop NC and Goosey-Tolfrey VL. Mucosal immune responses to treadmill exercise in elite wheelchair athletes. Med.Sci.Sports Exerc. 43: 1414-1421, 2011.
41. Leicht CA, Bishop NC, Paulson TAW, Griggs KE and Goosey-Tolfrey VL. Salivary immunoglobulin A and upper respiratory symptoms during five months of training in elite tetraplegic athletes. Int.J.Sports Physiol.Perform. 2011.
42. Lucin KM, Sanders VM, Jones TB, Malarkey WB and Popovich PG. Impaired antibody synthesis after spinal cord injury is level dependent and is due to sympathetic nervous system dysregulation. Exp.Neurol. 207: 75-84, 2007.
43. Lucin KM, Sanders VM and Popovich PG. Stress hormones collaborate to induce lymphocyte apoptosis after high level spinal cord injury. J.Neurochem. 110: 1409- 1421, 2009.
44. McHale NG and Thornbury KD. Sympathetic stimulation causes increased output of lymphocytes from the popliteal node in anaesthetized sheep. Exp.Physiol. 75: 847- 850, 1990.
45. Moynihan J, Kruszewska B, Madden K and Callahan T. Sympathetic nervous system regulation of immunity. J.Neuroimmunol. 147: 87-90, 2004.
46. Nagao F, Suzui M, Takeda K, Yagita H and Okumura K. Mobilization of NK cells by exercise: downmodulation of adhesion molecules on NK cells by catecholamines. Am.J.Physiol.Regul.Integr.Comp.Physiol. 279: R1251-6, 2000.
47. Nash MS. Immune dysfunction and illness susceptibility after spinal cord injury: An overview of probable causes, likely consequences, and potential treatments. J.Spinal Cord Med. 23: 109-110, 2000.
48. Nash MS. Known and plausible modulators of depressed immune functions following spinal cord injuries. J.Spinal Cord Med. 23: 111-120, 2000.
49. Nash MS. Immune responses to nervous system decentralization and exercise in quadriplegia. Med.Sci.Sports Exerc. 26: 164-171, 1994.
50. Nielsen S and Pedersen BK. Skeletal muscle as an immunogenic organ. Curr.Opin.Pharmacol. 8: 346-351, 2008.
51. Olive JL, Dudley GA and McCully KK. Vascular remodeling after spinal cord injury. Med.Sci.Sports Exerc. 35: 901-907, 2003.
52. Paulson TAW, Goosey-TolfreyVL, Lenton JP, Leicht CA and Bishop NC. Spinal cord injury level and the circulating cytokine response to strenuous exercise. Medicine and Science in Sports and Exercise 2013 DOI: 10.1249/MSS. 0b013e31828f9bbb.
53. Pavlov VA and Tracey KJ. Neural regulators of innate immune responses and inflammation. Cell Mol.Life Sci. 61: 2322-2331, 2004.
54. Paynter DE, Tipton CM and Tcheng TK. Response of immunosympathectomized rats to training. J.Appl.Physiol. 42: 935-940, 1977.
55. Pedersen BK. Muscles and their myokines. J.Exp.Biol. 214: 337-346, 2011.
56. Pedersen BK and Febbraio MA. Muscle as an endocrine organ: focus on musclederived interleukin-6. Physiol.Rev. 88: 1379-1406, 2008.
57. Proctor GB and Carpenter GH. Regulation of salivary gland function by autonomic nerves. Auton.Neurosci. 133: 3-18, 2007.
58. Proctor GB, Carpenter GH and Garrett JR. Sympathetic decentralization abolishes increased secretion of immunoglobulin A evoked by parasympathetic stimulation of rat submandibular glands. J.Neuroimmunol. 109: 147-154, 2000.
59. Proctor GB, Garrett JR, Carpenter GH and Ebersole LE. Salivary secretion of immunoglobulin A by submandibular glands in response to autonomimetic infusions in anaesthetised rats. J.Neuroimmunol. 136: 17-24, 2003.
60. Pyne DB, Gleeson M, McDonaldWA, Clancy RL, Perry C, Jr and Fricker PA. Training strategies to maintain immunocompetence in athletes. Int.J.Sports Med. 21 Suppl 1: S51-S60, 2000.
61. SchmidA, Huonker M, Barturen JM, Stahl F, Schmidt-TrucksassA, Konig D, Grathwohl D, Lehmann M and Keul J. Catecholamines, heart rate, and oxygen uptake during exercise in persons with spinal cord injury. J.Appl.Physiol. 85: 635-641, 1998.
62. Schmid A, Huonker M, Stahl F, Barturen JM, Konig D, Heim M, Lehmann M and Keul J. Free plasma catecholamines in spinal cord injured persons with different injury levels at rest and during exercise. J.Auton.Nerv.Syst. 68: 96-100, 1998.
63. Smith BM, Evans CT, Kurichi JE, Weaver FM, Patel N and Burns SP. Acute respiratory tract infection visits of veterans with spinal cord injuries and disorders: rates, trends, and risk factors. J.Spinal Cord Med. 30: 355-361, 2007.
64. Soden RJ, Walsh J, Middleton JW, Craven ML, Rutkowski SB and Yeo JD. Causes of death after spinal cord injury. Spinal Cord 38: 604-610, 2000.
65. Spence L, Brown WJ, Pyne DB, Nissen MD, Sloots TP, McCormack JG, Locke AS and Fricker PA. Incidence, etiology, and symptomatology of upper respiratory illness in elite athletes. Med.Sci.Sports Exerc. 39: 577-586, 2007.
66. Starkie RL, Rolland J and Febbraio MA. Effect of adrenergic blockade on lymphocyte cytokine production at rest and during exercise.Am.J.Physiol.Cell. Physiol. 281: C1233-40, 2001.
67. SteensbergA, Fischer CP, Keller C, Moller K and Pedersen BK. IL-6 enhances plasma IL- 1ra, IL-10, and cortisol in humans. Am.J.Physiol.Endocrinol. Metab. 285: E433-7, 2003.
68. Steensberg A, Toft AD, Schjerling P, Halkjaer-Kristensen J and Pedersen BK. Plasma interleukin-6 during strenuous exercise: role of epinephrine. Am.J.Physiol.Cell.Physiol. 281: C1001-4, 2001.
69. Steinberg LL, Lauro FA, Sposito MM, Tufik S, Mello MT, Naffah-Mazzacoratti MG, Cavalheiro EA and Silva AC. Catecholamine response to exercise in individuals with different levels of paraplegia. Braz.J.Med.Biol.Res. 33: 913-918, 2000.
70. Stolzmann KL, Gagnon DR, Brown R, Tun CG and Garshick E. Risk factors for chest illness in chronic spinal cord injury: A prospective study. Am.J.Phys.Med.Rehabil. 89: 576-583, 2010.
71. Tonnesen E, Christensen NJ and Brinklov MM. Natural killer cell activity during cortisol and adrenaline infusion in healthy volunteers. Eur.J.Clin.Invest. 17: 497- 503, 1987.
72. Ueta M, Furusawa K, Takahashi M, Akatsu Y, Nakamura T and Tajima F. Attenuation of natural killer cell activity during 2-h exercise in individuals with spinal cord injuries. Spinal Cord 46: 26-32, 2008.
73. Van Houtte S, VanlandewijckY and Gosselink R. Respiratory muscle training in persons with spinal cord injury: A systematic review. Respir.Med. 100: 1886-1895, 2006.
74. Vissing J, Wilson LB, Mitchell JH and Victor RG. Static muscle contraction reflexly increases adrenal sympathetic nerve activity in rats. Am.J.Physiol. 261: R1307-12, 1991.
75. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A and Simon P. Position statement. Part one: Immune function and exercise. Exerc.Immunol.Rev. 17: 6-63, 2011.
76. Wheeler G, Cumming D, Burnham R, Maclean I, Sloley BD, Bhambhani Y and Steadward RD. Testosterone, cortisol and catecholamine responses to exercise stress and autonomic dysreflexia in elite quadriplegic athletes. Paraplegia 32: 292-299, 1994.
77. Yamanaka M, Furusawa K, Sugiyama H, Goto M, Kinoshita T, Kanno N, Takaoka K and Tajima F. Impaired immune response to voluntary arm-crank ergometer exercise in patients with cervical spinal cord injury. Spinal Cord 48: 734-739, 2010.
78. Zeitzer JM, Ayas NT, Shea SA, Brown R and Czeisler CA. Absence of detectable melatonin and preservation of cortisol and thyrotropin rhythms in tetraplegia. J.Clin.Endocrinol.Metab. 85: 2189-2196, 2000.