Effect of lemon verbena supplementation on muscular damage markers, proinflammatory cytokines release and neutrophils’ oxidative stress in chronic exercise
- 592 Downloads
- 16 Citations
Abstract
Intense exercise is directly related to muscular damage and oxidative stress due to excessive reactive oxygen species (ROS) in both, plasma and white blood cells. Nevertheless, exercise-derived ROS are essential to regulate cellular adaptation to exercise. Studies on antioxidant supplements have provided controversial results. The purpose of this study was to determine the effect of moderate antioxidant supplementation (lemon verbena extract) in healthy male volunteers that followed a 90-min running eccentric exercise protocol for 21 days. Antioxidant enzymes activities and oxidative stress markers were measured in neutrophils. Besides, inflammatory cytokines and muscular damage were determined in whole blood and serum samples, respectively. Intense running exercise for 21 days induced antioxidant response in neutrophils of trained male through the increase of the antioxidant enzymes catalase, glutathione peroxidase and glutathione reductase. Supplementation with moderate levels of an antioxidant lemon verbena extract did not block this cellular adaptive response and also reduced exercise-induced oxidative damage of proteins and lipids in neutrophils and decreased myeloperoxidase activity. Moreover, lemon verbena supplementation maintained or decreased the level of serum transaminases activity indicating a protection of muscular tissue. Exercise induced a decrease of interleukin-6 and interleukin-1β levels after 21 days measured in basal conditions, which was not inhibited by antioxidant supplementation. Therefore, moderate antioxidant supplementation with lemon verbena extract protects neutrophils against oxidative damage, decreases the signs of muscular damage in chronic running exercise without blocking the cellular adaptation to exercise.
Keywords
Lippia citriodora Antioxidants Exercise Oxidative stress NeutrophilsNotes
Acknowledgments
We thank Monteloeder, S.L. for providing the lemon verbena extract and liability insurance. This investigation was awarded with the 2nd National Prize of Research in Sports Medicine 2009 (CajAstur), Spain. This investigation has been supported by Grants ACOMP/2010/107 from GV, and AGL2007-60778, AGL2007-62806, and FPI fellowship to L. Funes from Ministerio de Educación y Ciencia (MEC).
Conflict of interest
The authors declare that they have no conflict of interest.
References
- Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126PubMedCrossRefGoogle Scholar
- Baum M, Köpping-Menke K et al (1999) Increased concentrations of interleukin 1-beta in whole blood cultures supernatants after 12 weeks of moderate endurance exercise. Eur J Appl Physiol Occup Physiol 79(6):500–503PubMedCrossRefGoogle Scholar
- Davison G, Gleeson M et al (2007) Antioxidant supplementation and immunoendocrine responses to prolonged exercise. Med Sci Sports Exerc 39(4):645–652PubMedCrossRefGoogle Scholar
- Díaz AM, Abad MJ et al (2004) Phenylpropanoid glycosides from Scrophularia scorodonia: in vitro anti-inflammatory activity. Life Sci 74(20):2515–2526PubMedCrossRefGoogle Scholar
- Fallon KE, Sivyer G et al (1999) The biochemistry of runners in a 1600 km ultramarathon. Br J Sport Med 33(4):264–269CrossRefGoogle Scholar
- Ferrer MD, Tauler P et al (2009) Antioxidant regulatory mechanisms in neutrophils and lymphocytes after intense exercise. J Sports Sci 27(1):49–58PubMedCrossRefGoogle Scholar
- Fischer CP, Hiscock NJ et al (2004) Supplementation with vitamins C and E inhibits the release of interleukin-6 from contracting human skeletal muscle. J Physiol 558(2):633–645PubMedCrossRefGoogle Scholar
- Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121PubMedCrossRefGoogle Scholar
- Funes L, Fernández-Arroyo S et al (2009) Correlation between plasma antioxidant capacity and verbascoside levels in rats after oral administration of lemon verbena extract. Food Chem 117(4):589–598CrossRefGoogle Scholar
- Gleeson M (2007) Immune function in sport and exercise. J Appl Physiol 103(2):693–699PubMedCrossRefGoogle Scholar
- Goldberg DM, Spooner RJ (1983) Glutathione reductase. In: Bergmeyer HU, Bergmeyer J, Grabl M (eds) Methods of enzymatic analysis. Verlag Chemie, Basal, pp 258–265Google Scholar
- Gómez-Cabrera M-C, Domenech E et al (2008) Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87(1):142–149PubMedGoogle Scholar
- Hausmann M, Obermeier F et al (2007) In vivo treatment with the herbal phenylethanoid acteoside ameliorates intestinal inflammation in dextran sulphate sodium-induced colitis. Clin Exp Immunol 148(2):373–381PubMedCrossRefGoogle Scholar
- Ji LL (1995) Oxidative stress during exercise: implication of antioxidant nutrients. Free Radic Biol Med 18:1079–1086PubMedCrossRefGoogle Scholar
- Ji LL (2008) Modulation of skeletal muscle antioxidant defense by exercise: role of redox signaling. Free Radic Biol Med 44(2):142–152PubMedCrossRefGoogle Scholar
- Ji LL, Gómez-Cabrera MC et al (2004) Acute exercise activates nuclear factor (NF)-kappaB signaling pathway in rat skeletal muscle. Faseb J 18:1499–1506PubMedCrossRefGoogle Scholar
- Kim H, Lee Y et al (2007) Biomarkers of muscle and cartilage damage and inflammation during a 200 km run. Eur J Appl Physiol 99(4):443–447PubMedCrossRefGoogle Scholar
- Korkina LG, Mikhal’chik EV et al (2007) Molecular mechanisms underlying wound healing and anti-inflammatory properties of naturally occurring biotechnologically produced phenylpropanoid glycosides. Cell Mol Biol 53(5):84–91PubMedGoogle Scholar
- Lee JY, Woo ER et al (2005) Inhibition of lipopolysaccharide-inducible nitric oxide synthase expression by acteoside through blocking of AP-1 activation. J Ethnopharmacol 97(3):561–566PubMedCrossRefGoogle Scholar
- Levine RL, Williams JA et al (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357PubMedCrossRefGoogle Scholar
- Lin L-C, Wang Y-H et al (2006) The inhibitory effect of phenylpropanoid glycosides and iridoid glucosides on free radical production and beta2 integrin expression in human leucocytes. J Pharm Pharmacol 58(1):129–135PubMedCrossRefGoogle Scholar
- Liu MJ, Li JX et al (2003) The effects of verbascoside on plasma lipid peroxidation level and erythrocyte membrane fluidity during immobilization in rabbits: a time course study. Life Sci 73(7):883–892PubMedCrossRefGoogle Scholar
- McAnulty SR, McAnulty LS et al (2004) Consumption of blueberry polyphenols reduces exercise-induced oxidative stress compared to vitamin C. Nutr Res 24(3):209–221CrossRefGoogle Scholar
- McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055PubMedGoogle Scholar
- Miura M, Umeda T et al (2005) Effect of 6 months’ training on the reactive oxygen species production capacity of neutrophils and serum opsonic activity in judoists. Luminescence 20(1):1–7PubMedCrossRefGoogle Scholar
- Morillas-Ruiz J, Zafrilla P et al (2005) The effects of an antioxidant-supplemented beverage on exercise-induced oxidative stress: results from a placebo-controlled double-blind study in cyclists. Eur J Appl Physiol 95(5–6):543–549PubMedCrossRefGoogle Scholar
- Morillas-Ruiz JM, Villegas García JA et al (2006) Effects of polyphenolic antioxidants on exercise-induced oxidative stress. Clin Nutr 25(3):444–453PubMedCrossRefGoogle Scholar
- Morozov VI, Pryatkin SA et al (2003) Effect of exercise to exhaustion on myeloperoxidase and lysozyme release from blood neutrophils. Eur J Appl Physiol 89(3–4):257–262PubMedCrossRefGoogle Scholar
- Morozov VI, Tsyplenkov PV et al (2006) The effects of high-intensity exercise on skeletal muscle neutrophil myeloperoxidase in untrained and trained rats. Eur J Appl Physiol 97(6):716–722PubMedCrossRefGoogle Scholar
- Newall CA, Anderson LA, Phillipson JD (1996) Herbal medicines: a guide for health-care professionals. The Pharmaceutical Press, London, p 263Google Scholar
- Nieman D (1994) Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc 26:128–139PubMedCrossRefGoogle Scholar
- Nieman DC, Henson DA et al (2007) Quercetin’s influence on exercise-induced changes in plasma cytokines and muscle and leukocyte cytokine mRNA. J Appl Physiol 103(5):1728–1735PubMedCrossRefGoogle Scholar
- Noakes TD (1987) Effect of exercise on serum enzyme activities in humans. Sports Med 4(4):245–267PubMedCrossRefGoogle Scholar
- Panza VSP, Wazlawik E et al (2008) Consumption of green tea favorably affects oxidative stress markers in weight-trained men. Nutrition 24(5):433–442PubMedCrossRefGoogle Scholar
- Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev Suppl 80(3):1055–1081Google Scholar
- Pedersen BK, Toft AD (2000) Effects of exercise on lymphocytes and cytokines. Br J Sport Med 34(4):246–251CrossRefGoogle Scholar
- Petersen EW, Ostrowski K et al (2001) Effect of vitamin supplementation on cytokine response and on muscle damage after strenuous exercise. Am J Physiol Cell Physiol 280:C1570–C1575PubMedGoogle Scholar
- Phillips T, Childs AC et al (2003) A dietary supplement attenuates IL-6 and CRP after eccentric exercise in untrained males. Med Sci Sports Exerc 35(12):2032–2037PubMedCrossRefGoogle Scholar
- Quirantes-Piné R, Funes L et al (2009) High-performance liquid chromatography with diode array detection coupled to electrospray time-of-flight and ion-trap tandem mass spectrometry to identify phenolic compounds from a lemon verbena extract. J Chromatogr A 1216(28):5391–5397PubMedCrossRefGoogle Scholar
- Ristow M, Zarse K et al (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106(21):8665–8670PubMedCrossRefGoogle Scholar
- Su Q-S, Tian Y et al (2008) Effects of allicin supplementation on plasma markers of exercise-induced muscle damage, IL-6 and antioxidant capacity. Eur J Appl Physiol 103(3):275–283PubMedCrossRefGoogle Scholar
- Sureda A, Batle JM et al (2004a) Hypoxia/reoxygenation and vitamin C intake influence no synthesis and antioxidant defenses of neutrophils. Free Radic Biol Med 37(11):1744–1755PubMedCrossRefGoogle Scholar
- Sureda A, Batle JM et al (2004b) Neutrophil tolerance to oxidative stress induced by hypoxia/reoxygenation. Free Radic Res 38(9):1003–1009PubMedCrossRefGoogle Scholar
- Sureda A, Tauler P et al (2005) Relation between oxidative stress markers and antioxidant endogenous defences during exhaustive exercise. Free Radic Res 39(12):1317–1324PubMedCrossRefGoogle Scholar
- Sureda A, Ferrer MD et al (2007a) Intense physical activity enhances neutrophil antioxidant enzyme gene expression. Immunocytochemistry evidence for catalase secretion. Free Radic Res 41(8):874–883PubMedCrossRefGoogle Scholar
- Sureda A, Tauler P et al (2007b) Antioxidant supplementation influences the neutrophil tocopherol associated protein expression, but not the inflammatory response to exercise. Cent Eur J Biol 2(1):56–70CrossRefGoogle Scholar
- Sureda A, Tauler P et al (2008) Influence of an antioxidant vitamin-enriched drink on pre- and post-exercise lymphocyte antioxidant system. Ann Nutr Metab 52:233–240PubMedCrossRefGoogle Scholar
- Sureda A, Ferrer MD et al (2009) Effects of exercise intensity on lymphocyte H2O2 pro-duction and antioxidant defences in soccer players. Br J Sport Med 43:186–190CrossRefGoogle Scholar
- Suzuki K, Totsuka M et al (1999) Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol 87(4):1360–1367PubMedGoogle Scholar
- Tauler P, Aguiló A et al (2002a) Acute phase immune response to exercise coexists with decreased neutrophil antioxidant enzyme defences. Free Radic Res 36(10):1101–1107PubMedCrossRefGoogle Scholar
- Tauler P, Aguiló A et al (2002b) Diet supplementation with vitamin E, vitamin C and beta-carotene cocktail enhances basal neutrophil antioxidant enzymes in athletes. Pflugers Arch 443(5–6):791–797PubMedGoogle Scholar
- Tauler P, Aguiló A et al (2004) Different effects of exercise tests on the antioxidant enzyme activities in lymphocytes and neutrophils. J Nutr Biochem 15(8):479–484PubMedCrossRefGoogle Scholar
- Tauler P, Sureda A et al (2006) Increased lymphocyte antioxidant defences in response to exhaustive exercise do not prevent oxidative damage. J Nutr Biochem 17(10):665–671PubMedCrossRefGoogle Scholar
- Tauler P, Ferrer MD et al (2008) Supplementation with an antioxidant cocktail containing coenzyme Q prevents plasma oxidative damage induced by soccer. Eur J Appl Physiol 104(5):777–785PubMedCrossRefGoogle Scholar
- Urso ML, Clarkson PM (2003) Oxidative stress, exercise, and antioxidant supplementation. Toxicology 189(1–2):41–54PubMedCrossRefGoogle Scholar
- Valentao P, Fernandes E et al (2002) Studies on the antioxidant activity of Lippia citriodora infusion: scavenging effect on superoxide radical, hydroxyl radical and hypochlorous acid. Biol Pharm Bull 25(10):1324–1327PubMedCrossRefGoogle Scholar
- Vassilakopoulos T, Karatza MH et al (2003) Antioxidants attenuate the plasma cytokine response to exercise in humans. J Appl Physiol 94(3):1025–1032PubMedGoogle Scholar
- Yamada M, Suzuki K et al (2000) Effect of exhaustive exercise on human neutrophils in athletes. Luminescence 15(1):15–20PubMedCrossRefGoogle Scholar