Abstract
Exercise activates neutrophil burst and this effect is dependent on training status and exercise intensity. In this study, the chronic effect of treadmill exercise on phagocytosis, production of reactive oxygen metabolites and expression of NADPH oxidase components in rat neutrophils was investigated. Neutrophils were obtained by intraperitoneal lavage with PBS. After 11 weeks of training the exercised group showed increased phagocytosis capacity (49%) and production of reactive oxygen metabolites (6.6-fold) when compared with neutrophils from the sedentary group. Exercised had no effect on expression of the membrane components of NADPH oxidase (p22phox, gp91phox). In contrast, there was an increase of the p47phox mRNA levels (by 126%), the cytosolic component of the enzyme. In addition, exercise increased the protein content of p47phox (by 22%) and of p67phox (by 2.8-fold) in neutrophils. Evidence is then presented that training to moderate exercise increases phagocytosis and production of reactive oxygen metabolites and the expression of p47phox and p67phox in neutrophils. Therefore, moderate exercise might enable neutrophils to respond more efficiently when exposed to pathogens.
Similar content being viewed by others
References
Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16:42–47
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brooks GA, White TP (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol 45:1009–1015
Castell LM, Poortmans JR, Leclercq R, Brasseur M, Duchateau J, Newsholme EA (1997) Some aspects of the acute phase response after a marathon race, and the effects of glutamine supplementation. Eur J Appl Physiol Occup Physiol 75:47–53
Curi R, Lagranha CJ, Doi SQ, Sellitti DF, Procopio J, Pithon-Curi TC, Corless M, Newsholme P (2005) Molecular mechanisms of glutamine action. J Cell Physiol 204:392–401
Freund BJ, Claybaugh JR, Hashiro GM, Buono M, Chrisney S (1990) Exaggerated ANF response to exercise in middle-aged vs. young runners. J Appl Physiol 69:1607–1614
Furukawa S, Saito H, Inoue T, Matsuda T, Fukatsu K, Han I, Ikeda S, Hidemura A (2000) Supplemental glutamine augments phagocytosis and reactive oxygen intermediate production by neutrophils and monocytes from postoperative patients in vitro. Nutrition 16:323–329
Hack V, Strobel G, Rau JP, Weicker H (1992) The effect of maximal exercise on the activity of neutrophil granulocytes in highly trained athletes in a moderate training period. Eur J Appl Physiol Occup Physiol 65:520–524
Hsu TG, Hsu KM, Kong CW, Lu FJ, Cheng H, Tsai K (2002) Leukocyte mitochondria alterations after aerobic exercise in trained human subjects. Med Sci Sports Exerc 34:438–442
Ikeda S, Kudsk KA, Le T, Zarzaur BL, Johnson CD (2003) Glutamine improves impaired cellular exudation and polymorphonuclear neutrophil phagocytosis induced by total parenteral nutrition after glycogen-induced murine peritonitis. Shock 19:50–54
Inder WJ, Hellemans J, Swanney MP, Prickett TC, Donald RA (1998) Prolonged exercise increases peripheral plasma ACTH, CRH, and AVP in male athletes. J Appl Physiol 85:835–841
Kargotich S, Goodman C, Dawson B, Morton AR, Keast D, Joske DJ (2005) Plasma glutamine responses to high-intensity exercise before and after endurance training. Res Sports Med (Print) 13:287–300
Kowatari K, Umeda T, Shimoyama T, Nakaji S, Yamamoto Y, Sugawara K (2001) Exercise training and energy restriction decrease neutrophil phagocytic activity in judoists. Med Sci Sports Exerc 33:519–524
Lagranha CJ, Senna SM, de Lima TM, Silva EP, Doi SQ, Curi R, Pithon-Curi TC (2004) Beneficial effect of glutamine on exercise-induced apoptosis of rat neutrophils. Med Sci Sports Exerc 36:210–217
Lagranha CJ, de Lima TM, Senna SM, Doi SQ, Curi R, Pithon-Curi TC (2005) The effect of glutamine supplementation on the function of neutrophils from exercised rats. Cell Biochem Funct 23:101–107
Leandro CG, Martins de Lima T, Folador A, Alba Loreiro T, do Nascimento E, Manhaes de Castro R, de Castro CM, Pithon-Curi T, Curi R (2006) Physical training attenuates the stress-induced changes in rat T-lymphocyte function. Neuroimmunomodulation 13(2):105–113
Matthews CE, Ockene IS, Freedson PS, Rosal MC, Merriam PA, Hebert JR (2002) Moderate to vigorous physical activity and risk of upper-respiratory tract infection. Med Sci Sports Exerc 34:1242–1248
Meyer T, Gabriel HH, Ratz M, Muller HJ, Kindermann W (2001) Anaerobic exercise induces moderate acute phase response. Med Sci Sports Exerc 33:549–555
Nieman DC (1994a) Exercise, infection, and immunity. Int J Sports Med 15(suppl 3):S131–S141
Nieman DC (1994b) Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc 26:128–139
Ortega E (2003) Neuroendocrine mediators in the modulation of phagocytosis by exercise: physiologicaal implications. Exerc Immunol Rev 9:70–93
Ostrowski K, Schjerling P, Pedersen BK (2000) Physical activity and plasma interleukin-6 in humans–effect of intensity of exercise. Eur J Appl Physiol 83:512–515
Peake JM (2002) Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc Immunol Rev 8:49–100
Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombes JS (2005) Plasma cytokine changes in relation to exercise intensity and muscle damage. Eur J Appl Physiol 95:514–521
Pithon-Curi TC, Levada AC, Lopes LR, Doi SQ, Curi R (2002) Glutamine plays a role in superoxide production and the expression of p47phox, p22phox and gp91phox in rat neutrophils. Clin Sci (Lond) 103:403–408
Pithon-Curi TC, Schumacher RI, Freitas JJ, Lagranha C, Newsholme P, Palanch AC, Doi SQ, Curi R (2003) Glutamine delays spontaneous apoptosis in neutrophils. Am J Physiol 284:C1355–C1361
Pyne DB (1994) Regulation of neutrophil function during exercise. Sports Med 17:245–258
Pyne DB, Baker MS, Fricker PA, McDonald WA, Telford RD, Weidemann MJ (1995) Effects of an intensive 12-wk training program by elite swimmers on neutrophil oxidative activity. Med Sci Sports Exerc 27:536–542
Quinn MT, Ammons MC, Deleo FR (2006) The expanding role of NADPH oxidases in health and disease: no longer just agents of death and destruction. Clin Sci (Lond) 111:1–20
Robson PJ, Blannin AK, Walsh NP, Castell LM, Gleeson M (1999) Effects of exercise intensity, duration and recovery on in vitro neutrophil function in male athletes. Int J Sports Med 20:128–135
Rothe G, Valet G (1990) Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′-dichlorofluorescin. J Leukoc Biol 47:440–448
Shapiro AL, Vinuela E, Maizel JV Jr (1967) Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun 28:815–820
Smith JA, Telford RD, Mason IB, Weidemann MJ (1990) Exercise, training and neutrophil microbicidal activity. Int J Sports Med 11:179–187
Struder HK, Hollmann W, Platen P, Wostmann R, Ferrauti A, Weber K (1997) Effect of exercise intensity on free tryptophan to branched-chain amino acids ratio and plasma prolactin during endurance exercise. Can J Appl Physiol (Revue Canadienne de Physiologie Appliquee) 22:280–291
Suzuki K, Totsuka M, Nakaji S, Yamada M, Kudoh S, Liu Q, Sugawara K, Yamaya K, Sato K (1999) Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol 87:1360–1367
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354
Vazquez-Torres A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J Exp Med 192:227–236
Wang JS, Huang YH (2005) Effects of exercise intensity on lymphocyte apoptosis induced by oxidative stress in men. Eur J Appl Physiol 95:290–297
Weltman A, Pritzlaff CJ, Wideman L, Weltman JY, Blumer JL, Abbott RD, Hartman ML, Veldhuis JD (2000) Exercise-dependent growth hormone release is linked to markers of heightened central adrenergic outflow. J Appl Physiol 89:629–635
Acknowledgments
The authors are grateful to JR Mendonça, EPP Santos, and G de Souza, for technical assistance. FAPESP, CNPq and CAPES support this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Levada-Pires, A.C., Lambertucci, R.H., Mohamad, M. et al. Exercise training raises expression of the cytosolic components of NADPH oxidase in rat neutrophils. Eur J Appl Physiol 100, 153–160 (2007). https://doi.org/10.1007/s00421-007-0414-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-007-0414-y