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Published in: European Journal of Applied Physiology 1/2009

01-09-2009 | Original Article

Exercise-induced elevation in plasma oxidative generating capability augments the temporal inflammatory response stimulated by lipopolysaccharide

Authors: Suzanne Maria Hurst, K. A. Lyall, R. D. Hurst, L. M. Stevenson

Published in: European Journal of Applied Physiology | Issue 1/2009

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Abstract

Prolonged oxidative stress is detrimental to health; however, transient oxidative stress may improve immune capability. We examined whether exercise-induced increases in the plasma oxidative generating capability enhance immune responsiveness to potential pathogens. Twelve individuals underwent a 30-min row and pre and post-exercise bloods were collected for oxidative stress and immune assessment. We found that exercise induced a transient increase in plasma carbonyls (3.2–5.3 nmol/mg protein) and creatine kinase activity (0.5–1.2 absorbance/min/mg protein) and that lipopolysaccharide (LPS) stimulation (0.5–24 h) of pre- and post-exercise blood augmented temporal tumour necrosis factor-α (TNFα) secretion. Further characterisation of plasma using a modified dihydro-2′,7′-dichlorohydrofluorescein (DCF) assay revealed that addition of a sub-threshold of hydrogen peroxide to post-exercise (and not pre-exercise) plasma caused a sixfold increase in the radical oxygen species (ROS) generating capability after 15 min (555 ± 131 to 3607 ± 488 change in fluorescent intensity [ΔFI]), which was inhibited using 60 mM N-acetyl-l-cysteine (920 ± 154 ΔFI). Furthermore, cell experiments revealed that LPS stimulation of either THP-1 cells pre-incubated with post-exercise plasma or peripheral blood mononuclear cells pre-treated with pro-oxidants, modulated the temporal secretion of key cytokines that regulate the initiation, progression and resolution of an inflammatory response. These results indicate that exercise-induced changes in plasma parameters (e.g. oxidative generating capability—dependent or independent of inflammatory mediators) augment the temporal LPS response and support the notion that repeated transient oxidative stress (such as that induced by regular exercise) is important for a “healthy” immune system.
Literature
go back to reference Childs A, Jacobs C, Kaminski T, Halliwell B, Leeuwenburgh C (2001) Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after acute muscle injury induced by eccentric exercise. Free Radic Biol Med 31(6):745–753. doi:10.1016/50891-5849(01)00640-2 PubMedCrossRef Childs A, Jacobs C, Kaminski T, Halliwell B, Leeuwenburgh C (2001) Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after acute muscle injury induced by eccentric exercise. Free Radic Biol Med 31(6):745–753. doi:10.​1016/​50891-5849(01)00640-2 PubMedCrossRef
go back to reference Den Broeder AA, Wanten GJA, Oyen WJG, Naber T, Van Riel PL, Barrera P (2003) Neutrophil migration and production of reactive oxygen species during treatment with a fully human anti-tumor necrosis factor-α monoclonal antibody in patients with rheumatoid arthritis. J Rheumatol 30(2):232–237 Den Broeder AA, Wanten GJA, Oyen WJG, Naber T, Van Riel PL, Barrera P (2003) Neutrophil migration and production of reactive oxygen species during treatment with a fully human anti-tumor necrosis factor-α monoclonal antibody in patients with rheumatoid arthritis. J Rheumatol 30(2):232–237
go back to reference German Society for Clinical Chemistry (1977) Standardization of methods for the determination of creatine kinase activity. Eur J Clin Chem Biochem 15:255–260 German Society for Clinical Chemistry (1977) Standardization of methods for the determination of creatine kinase activity. Eur J Clin Chem Biochem 15:255–260
go back to reference Karvonen M, Kentala K, Mustala O (1957) The effects of training on heart rate: a longitudinal study. Ann Med Exp Biol Fenn 35:307–315PubMed Karvonen M, Kentala K, Mustala O (1957) The effects of training on heart rate: a longitudinal study. Ann Med Exp Biol Fenn 35:307–315PubMed
go back to reference Li N, Karin M (1999) Is NF-κB the sensor for oxidative stress? FASEB J 13:1137PubMed Li N, Karin M (1999) Is NF-κB the sensor for oxidative stress? FASEB J 13:1137PubMed
go back to reference Morabito F, Tomaino A, Cristani M, Cimino F, Martino A, Minciullo PL, Calabro C, Saija A, Gangemi S (2005) Modification of the content of plasma protein carbonyl groups in donors after granulocyte colony stimulating factor-induced stem cell mobilization. Trans Aphereis Sci 33:141–146. doi:10.1016/j.transci.2005.05.003 CrossRef Morabito F, Tomaino A, Cristani M, Cimino F, Martino A, Minciullo PL, Calabro C, Saija A, Gangemi S (2005) Modification of the content of plasma protein carbonyl groups in donors after granulocyte colony stimulating factor-induced stem cell mobilization. Trans Aphereis Sci 33:141–146. doi:10.​1016/​j.​transci.​2005.​05.​003 CrossRef
go back to reference Nieman DC, Henson DA, McAnulty SR, McAnulty L, Swick NS, Utter AC, Vinci DM, Opiela SJ, Morrow JD (2002) Influence of vitamin C supplementation on oxidative and immune changes after an ultramarathon. J Appl Physiol 92:1970–1977. doi:10.1152/japplphysiol.00961.2001 PubMed Nieman DC, Henson DA, McAnulty SR, McAnulty L, Swick NS, Utter AC, Vinci DM, Opiela SJ, Morrow JD (2002) Influence of vitamin C supplementation on oxidative and immune changes after an ultramarathon. J Appl Physiol 92:1970–1977. doi:10.​1152/​japplphysiol.​00961.​2001 PubMed
go back to reference Oliver IT (1955) A spectrophotometric method for the determination of creatine phosphokinase and myokinase. Biochem J 61:116PubMed Oliver IT (1955) A spectrophotometric method for the determination of creatine phosphokinase and myokinase. Biochem J 61:116PubMed
go back to reference Rogers PJ, Tyce GM, Weinshilboum RM, O’Connor DT, Bailey KR, Bove AA (1991) Catecholamine metabolic pathways and exercise training. Plasma and urine catecholamines, metabolic enzymes and chromogranin-A. Circulation 84:2346–2356PubMed Rogers PJ, Tyce GM, Weinshilboum RM, O’Connor DT, Bailey KR, Bove AA (1991) Catecholamine metabolic pathways and exercise training. Plasma and urine catecholamines, metabolic enzymes and chromogranin-A. Circulation 84:2346–2356PubMed
go back to reference Starkie RL, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK (2003) Exercise and IL-6 infusion inhibits endotoxin-induced TNFα production in humans. FASEB J 17:884–886. doi:10.1096/fj.02-0670fje PubMed Starkie RL, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK (2003) Exercise and IL-6 infusion inhibits endotoxin-induced TNFα production in humans. FASEB J 17:884–886. doi:10.​1096/​fj.​02-0670fje PubMed
go back to reference Vider J, Lehtmaa J, Kullisaar T, Vihalemm T, Zilmer K, Kairane C, Landor A, Zilmer M (2001) Acute mmune response in respect to exercise-induced oxidative stress. Path Physiol 7:263–270. doi:10.1016/S0928-4680(00)00057-2 Vider J, Lehtmaa J, Kullisaar T, Vihalemm T, Zilmer K, Kairane C, Landor A, Zilmer M (2001) Acute mmune response in respect to exercise-induced oxidative stress. Path Physiol 7:263–270. doi:10.​1016/​S0928-4680(00)00057-2
Metadata
Title
Exercise-induced elevation in plasma oxidative generating capability augments the temporal inflammatory response stimulated by lipopolysaccharide
Authors
Suzanne Maria Hurst
K. A. Lyall
R. D. Hurst
L. M. Stevenson
Publication date
01-09-2009
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 1/2009
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-009-1099-1

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