A pediatric perspective on inflammation and oxidative stress in response to exercise

Applied Physiology, Nutrition and Metabolism

Volumn 33, Issue 2, 2008, Pages 411-419

  Timmons, Brian W ^a   Raha, Sandeep ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Children; Cytokines; Exercise; Oxidative stress

Indexed keywords

CYTOKINE;

CHILD; CONFERENCE PAPER; EXERCISE; HUMAN; INFLAMMATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

CHILD; CYTOKINES; EXERCISE; HUMANS; INFLAMMATION; OXIDATIVE STRESS;

EID: 41649100669     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H07-183     Document Type: Conference Paper

References (65)

1. Akerstrom, T., Steensberg, A., Keller, P., Keller, C., Penkowa, M., and Pedersen, B.K. 2005. Exercise induces interleukin-8 expression in human skeletal muscle. J. Physiol. 563: 507-516. doi:10.1113/jphysiol.2004.077610.
2. Boas, S.R., Joswiak, M.L., Nixon, P.A., Kurland, G., O'Connor, M.J., Bufalino, K., et al. 1996. Effects of anaerobic exercise on the immune system in eight- to seventeen-year-old trained and untrained boys. J. Pediatr. 129: 846-855. doi:10.1016/S0022-3476(96)70028-8.
3. Bruunsgaard, H. 2005. Physical activity and modulation of systemic low-level inflammation. J. Leukoc. Biol. 78: 819-835. doi:10.1189/jlb.0505247.
4. Chan, M.H.S., Carey, A.L., Watt, M.J., and Febbraio, M.A. 2004. Cytokine gene expression in human skeletal muscle during concentric contraction: evidence that IL-8, like IL-6, is influenced by glycogen availability. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287: R322-R327.
5. Cohen, T., Nahari, D., Cerem, L.W., Neufeld, G., and Levi, B.Z. 1996. Interleukin 6 induces the expression of vascular endothelial growth factor. J. Biol. Chem. 271: 736-741. doi:10.1074/jbc.271.2.736.
6. Colombo, C., Costantini, D., Rocchi, A., Cariani, L., Garlaschi, M.L., Tirelli, S., et al. 2005. Cytokine levels in sputum of cystic fibrosis patients before and after antibiotic therapy. Pediatr. Pulmonol. 40: 15-21. doi:10.1002/ppul.20237.
7. Cunningham, S., McColm, J.R., Mallinson, A., Boyd, I., and Marshall, T.G. 2003. Duration of effect of intravenous antibiotics on spirometry and sputum cytokines in children with cystic fibrosis. Pediatr. Pulmonol. 36: 43-48. doi:10.1002/ppul.10311.
8. de Benedetti, F., Alonzi, T., Moretta, A., Lazzaro, D., Costa, P., Poli, V., et al. 1997. Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation. J. Clin. Invest. 99: 643-650.
9. Duarte, J.A., Magalhaes, J.F., Monteiro, L., Almeida-Dias, A., Soares, J.M., and Appell, H.J. 1999. Exercise-induced signs of muscle overuse in children. Int. J. Sports Med. 20: 103-108. doi:10.1055/s-2007-971101.
10. Dumaswala, U.J., Zhuo, L., Jacobsen, D.W., Jain, S.K., and Sukalski, K.A. 1999. Protein and lipid oxidation of banked human erythrocytes: role of glutathione. Free Radic. Biol. Med. 27: 1041-1049. doi:10.1016/S0891- 5849(99)00149-5.
11. Eberhardt, W., Beck, K.F., and Pfeilschifter, J. 2002. Cytokine-induced expression of tPA is differentially modulated by NO and ROS in rat mesangial cells. Kidney Int. 61: 20-30. doi:10.1046/j.1523-1755.2002.00087.x.
12. Eliakim, A., Wolach, B., Kodesh, E., Gavrieli, R., Radnay, J., Ben Tovim, T., et al. 1997. Cellular and humoral immune response to exercise among gymnasts and untrained girls. Int. J. Sports Med. 18: 208-212. doi:10.1055/s-2007-972621.
13. Fibbe, W.E., Pruijt, J.F., Velders, G.A., Opdenakker, G., van Kooyk, Y., Figdor, C.G., et al. 1999. Biology of IL-8-induced stem cell mobilization. Ann. N. Y. Acad. Sci. 872: 71-82. doi:10.1111/j.1749-6632.1999.tb08454.x.
14. Galassetti, P.R., Iwanaga, K., Crisostomo, M., Zaldivar, F.P., Larson, J., and Pescatello, A. 2006. Inflammatory cytokine, growth factor and counterregulatory responses to exercise in children with type 1 diabetes and healthy controls. Pediatr. Diabetes, 7: 16-24. doi:10.1111/j.1399-543X. 2006.00140.x.
15. Gomez-Cabrera, M.C., Borras, C., Pallardo, F.V., Sastre, J., Ji, L.L., and Vina, J. 2005. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J. Physiol. 567: 113-120. doi:10.1113/jphysiol.2004.080564.
16. Grohmann, M., Foulstone, E., Welsh, G., Holly, J., Shield, J., Crowne, E., et al. 2005. Isolation and validation of human prepubertal skeletal muscle cells: maturation and metabolic effects of IGF-I, IGFBP-3 and TNFa. J. Physiol. 568: 229-242. doi:10.1113/jphysiol.2005.093906.
17. Hotamisligil, G.S., Arner, P., Caro, J.F., Atkinson, R.L., and Spiegelman, B.M. 1995. Increased adipose tissue expression of tumor necrosis factor-a in human obesity and insulin resistance. J. Clin. Invest. 95: 2409-2415.
18. Hughes, G., Murphy, M.P., and Ledgerwood, E.C. 2005. Mitochondrial reactive oxygen species regulate the temporal activation of nuclear factor kB to modulate tumour necrosis factor-induced apoptosis: evidence from mitochondria-targeted antioxidants. Biochem. J. 389: 83-89. doi:10.1042/BJ20050078.
19. Jackson, M.J. 2005. Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360: 2285-2291. doi:10.1098/rstb.2005.1773.
20. Ji, L.L., Gomez-Cabrera, M.C., and Vina, J. 2006. Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann. N. Y. Acad. Sci. 1067: 425-435. doi:10.1196/annals.1354.061.
21. Judge, A.R., and Dodd, S.L. 2004. Xanthine oxidase and activated neutrophils cause oxidative damage to skeletal muscle after contractile claudication. Am. J. Physiol. Heart Circ. Physiol. 286: H252-H256. doi:10.1152/ajpheart.00684.2003.
22. Kern, P.A., Saghizadeh, M., Ong, J.M., Bosch, R.J., Deem, R., and Simsolo, R.B. 1995. The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J. Clin. Invest. 95: 2111-2119.
23. Laaksonen, D.E., Atalay, M., Niskanen, L., Uusitupa, M., Hanninen, O., and Sen, C.K. 1999. Blood glutathione homeostasis as a determinant of resting and exercise-induced oxidative stress in young men. Redox Rep. 4: 53-59. doi:10.1179/135100099101534648.
24. Lang, C.H., Frost, R.A., Nairn, A.C., MacLean, D.A., and Vary, T.C. 2002. TNF-a impairs heart and skeletal muscle protein synthesis by altering translation initiation. Am. J. Physiol. Endocrinol. Metab. 282: E336-E347.
25. Mahoney, D.J., Parise, G., Melov, S., Safdar, A., and Tarnopolsky, M.A. 2005. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 19: 1498-1500.
26. Majka, M., Janowska-Wieczorek, A., Ratajczak, J., Ehrenman, K., Pietrzkowski, Z., Kowalska, M.A., et al. 2001. Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood, 97: 3075-3085. doi:10.1182/blood.V97. 10.3075.
27. McMurray, R.G., Zaldivar, F., Galassetti, P., Larson, J., Eliakim, A., Nemet, D., et al. 2007. Cellular immunity and inflammatory mediator responses to intense exercise in overweight children and adolescents. J. Investig. Med. 55: 120-129. doi:10.2310/6650.2007.06031.
28. Meyer, A.A., Kundt, G., Lenschow, U., Schuff-Werner, P., and Kienast, W. 2006. Improvement of early vascular changes and cardiovascular risk factors in obese children after a six-month exercise program. J. Am. Coll. Cardiol. 48: 1865-1870. doi:10.1016/j.jacc.2006.07.035.
29. Mohn, A., Catino, M., Capanna, R., Giannini, C., Marcovecchio, M., and Chiarelli, F. 2005. Increased oxidative stress in prepubertal severely obese children: effect of a dietary restriction-weight loss program. J. Clin. Endocrinol. Metab. 90: 2653-2658. doi:10.1210/jc.2004-2178.
30. Mohn, A., Chiavaroli, V., Cerruto, M., Blasetti, A., Giannini, C., Bucciarelli, T., et al. 2007. Increased oxidative stress in prepubertal children born small for gestational age. J. Clin. Endocrinol. Metab. 92: 1372-1378. doi:10.1210/jc.2006-1344.
31. Moller, D.E. 2000. Potential role of TNF-α in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrinol. Metab. 11: 212-217. doi:10.1016/S1043-2760(00)00272-1.
32. 2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc. Natl. Acad. Sci. U.S.A. 87: 9383-9387. doi:10.1073/pnas.87.23.9383.
33. Mukherjee, T.K., Mukhopadhyay, S., and Hoidal, J.R. 2005. The role of reactive oxygen species in TNFα-dependent expression of the receptor for advanced glycation end products in human umbilical vein endothelial cells. Biochim. Biophys. Acta, 1744: 213-223. doi:10.1016/j.bbamcr.2005.03.007.
34. Nemet, D., Oh, Y., Kim, H.S., Hill, M., and Cooper, D.M. 2002. Effect of intense exercise on inflammatory cytokines and growth mediators in adolescent boys. Pediatrics, 110: 681-689. doi:10.1542/peds.110.4.681.
35. Nemet, D., Rose-Gottron, C.M., Mills, P.J., and Cooper, D.M. 2003. Effect of water polo practice on cytokines, growth mediators, and leukocytes in girls. Med. Sci. Sports Exerc. 35: 356-363. doi:10.1249/01.MSS.0000048722. 84182.E3.
36. Nieman, D.C., Kernodle, M.W., Henson, D.A., Sonnenfeld, G., and Morton, D.S. 2000. The acute response of the immune system to tennis drills in adolescent athletes. Res. Q. Exerc. Sport, 71: 403-408.
37. Nikolaidis, M.G., Kyparos, A., Hadziioannou, M., Panou, N., Samaras, L., Jamurtas, A.Z., et al. 2007. Acute exercise markedly increases blood oxidative stress in boys and girls. Appl. Physiol. Nutr. Metab. 32: 197-205. doi:10.1139/H06-097.
38. Ou, L.S., See, L.C., Wu, C.J., Kao, C.C., Lin, Y.L., and Huang, J.L. 2002. Association between serum inflammatory cytokines and disease activity in juvenile idiopathic arthritis. Clin. Rheumatol. 21: 52-56. doi:10.1007/s100670200012.
39. Palermo, A.T., LaBarge, M.A., Doyonnas, R., Pomerantz, J., and Blau, H.M. 2005. Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev. Biol. 279: 336-344. doi:10.1016/j.ydbio.2004.12.024.
40. Perez Navero, J.L., Jaraba Caballero, S., Ibarra de la Rosa, I., Jaraba Caballero, M.P., Guillen del Castillo, M., Montilla Lopez, P., Tunez Finana, I., and Romanos Lezcano, A. 1999. Effects of competitive physical exercise on neuroendocrine response and interleukin-6 liberation in children. An. Esp. Pediatr. 51: 267-272.
41. Petersen, A.M., and Pedersen, B.K. 2005. The anti-inflammatory effect of exercise. J. Appl. Physiol. 98: 1154-1162. doi:10.1152/japplphysiol. 00164.2004.
42. Raha, S., McEachern, G.E., Myint, A.T., and Robinson, B.H. 2000. Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Radic. Biol. Med. 29: 170-180. doi:10.1016/S0891-5849(00) 00338-5.
43. Raha, S., and Robinson, B.H. 2000. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25: 502-508. doi:10.1016/S0968-0004(00)01674-1.
44. Raha, S., and Robinson, B.H. 2003. Metabolic actions of free radicals: Walking the tightrope. Heart Metab., 19: 4-10.
45. Reid, M.B. 2001. Redox modulation of skeletal muscle contraction: what we know and what we don't. J. Appl. Physiol. 90: 724-731. doi:10.1063/1.1381002.
46. Reid, M.B., and Li, Y.P. 2001. Cytokine and oxidative signalling in skeletal muscle. Acta Physiol. Scand. 171: 225-232. doi:10.1046/j.1365- 201x.2001.00824.x.
47. Rodriguez, M.C., and Tarnopolsky, M.A. 2003. Patients with dystrophinopathy show evidence of increased oxidative stress. Free Radic. Biol. Med. 34: 1217-1220. doi:10.1016/S0891-5849(03)00141-2.
48. Ryan, K.A., Smith, M.F., Jr., Sanders, M.K., and Ernst, P.B. 2004. Reactive oxygen and nitrogen species differentially regulate Toll-like receptor 4-mediated activation of NF-κB and interleukin-8 expression. Infect. Immun. 72: 2123-2130. doi:10.1128/IAI.72.4.2123-2130.2004.
49. Sastre, J., Asensi, M., Gasco, E., Pallardo, F.V., Ferrero, J.A., Furukawa, T., et al. 1992. Exhaustive physical exercise causes oxidation of glutathione status in blood: prevention by antioxidant administration. Am. J. Physiol. 263: R992-R995.
50. Scheett, T.P., Mills, P.J., Ziegler, M.G., Stoppani, J., and Cooper, D.M. 1999. Effect of exercise on cytokines and growth mediators in prepubertal children. Pediatr. Res. 46: 429-434. doi:10.1203/00006450-199910000- 00011.
51. Sen, C.K. 1999. Glutathione homeostasis in response to exercise training and nutritional supplements. Mol. Cell. Biochem. 196: 31-42. doi:10.1023/A:1006910011048.
52. 2 release by subsarcolemmal and intermyofibrillar mitochondria. Free Radic. Biol. Med. 35: 24-32. doi:10.1016/S0891- 5849(03)00177-1.
53. Shahin, A.A., Shaker, O.G., Kamal, N., Hafez, H.A., Gaber, W., and Shahin, H.A. 2002. Circulating interleukin-6, soluble interleukin-2 receptors, tumor necrosis factor α, and interleukin-10 levels in juvenile chronic arthritis: correlations with soft tissue vascularity assessed by power Doppler sonography. Rheumatol. Int. 22: 84-88. doi:10.1007/s00296-002-0191-1.
54. Starkie, R., Ostrowski, S.R., Jauffred, S., Febbraio, M., and Pedersen, B.K. 2003. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-α production in humans. FASEB J. 17: 884-886.
55. Steensberg, A., Van Hall, G., Osada, T., Sacchetti, M., Saltin, B., and Klarlund, P.B. 2000. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J. Physiol. 529: 237-242. doi:10.1111/j.1469-7793.2000.00237.x.
56. Timmons, B.W. 2005a. Immune responses to exercise in children: a brief review. Pediatr. Exerc. Sci. 18: 290-299.
57. Timmons, B.W. 2005b. Paediatric exercise immunology: health and clinical applications. Exerc. Immunol. Rev. 11: 108-144.
58. Timmons, B.W. 2006. Exercise and the cytokine balance: a paediatric perspective. J. Sports Sci. 24: 1-2. doi:10.1080/02640410500456705.
59. Timmons, B.W., Tarnopolsky, M.A., and Bar-Or, O. 2004. Immune responses to strenuous exercise and carbohydrate intake in boys and men. Pediatr. Res. 56: 227-234. doi:10.1203/01.PDR.0000132852.29770.C5.
60. Timmons, B.W., Tarnopolsky, M.A., Snider, D.P., and Bar-Or, O. 2006. Immunological changes in response to exercise: influence of age, puberty, and gender. Med. Sci. Sports Exerc. 38: 293-304. doi:10.1249/01.mss. 0000183479.90501.a0.
61. Tirakitsoontorn, P., Nussbaum, E., Moser, C., Hill, M., and Cooper, D.M. 2001. Fitness, acute exercise, and anabolic and catabolic mediators in cystic fibrosis. Am. J. Respir. Crit. Care Med. 164: 1432-1437.
62. Ustundag, B., Gungor, S., Aygun, A.D., Turgut, M., and Yilmaz, E. 2007. Oxidative status and serum leptin levels in obese prepubertal children. Cell Biochem. Funct. 25: 479-483. doi:10.1002/cbf.1334.
63. Vasilaki, A., Mansouri, A., Remmen, H., van der Meulen, J.H., Larkin, L., Richardson, A.G., et al. 2006. Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell, 5: 109-117. doi:10.1111/j.1474-9726.2006.00198.x.
64. Vassilakopoulos, T., Karatza, M.H., Katsaounou, P., Kollintza, A., Zakynthinos, S., and Roussos, C. 2003. Antioxidants attenuate the plasma cytokine response to exercise in humans. J. Appl. Physiol. 94: 1025-1032.
65. Wright, D.C., Han, D.H., Garcia-Roves, P.M., Geiger, P.C., Jones, T.E., and Holloszy, J.O. 2007. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1a expression. J. Biol. Chem. 282: 194-199. doi:10.1074/jbc.M606116200.