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Published in: Journal of the International Society of Sports Nutrition 1/2016

Open Access 01-12-2016 | Research article

Effects of dietary Docosahexaenoic, training and acute exercise on lipid mediators

Authors: X. Capó, M. Martorell, A. Sureda, J. A. Tur, A. Pons

Published in: Journal of the International Society of Sports Nutrition | Issue 1/2016

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Abstract

Background

Eicosanoids mediate initiation and resolution of inflammation. Our aim was evaluating the effects of training, exercise and docosahexaenoic (DHA) supplementation on plasma eicosanoids levels and peripheral blood mononuclear cells (PBMCs) eicosanoids production.

Methods

Fifteen male footballers were distributed to placebo and experimental groups. Experimental group consumed DHA-enriched beverage (1.16 g DHA/day) for 8 weeks, placebo group consumed a placebo beverage. Blood samples were taken before and after the nutritional intervention in basal conditions and 2 h after acute exercise.

Results

Training increased basal Prostaglandin E1 (PGE1) plasma levels and PBMCs cyclooxygenase 2 (COX-2) protein levels in both groups, but COX-1 protein levels only in the experimental group. Acute exercise increased plasma PGE2 and PBMCs active NFκβ levels. Lipopolysaccharide (LPS)-stimulated PBMCs increases eicosanoids production (PGE1, PGE2, RvD1) in both groups and increased LPS-stimulated PBMCs active NFκβ. DHA supplementation increased COX-2 levels but decreased LPS-stimulated PBMCs PGE1 and PGE2 production. Neither DHA supplementation nor acute exercise altered the expression of NFκβ, COX-2, 15-LOX2, 5-LOX, or IL-1β genes in PBMCs.

Conclusions

The increase of PGE1 plasma levels after training promoted systemic anti-inflammatory and vasodilator environment. Exercise and DHA supplementation acted synergistically by increasing plasma PGE2 with anti-inflammatory effects. Exercise primed PBMCs to enhance PGE1, PGE2 and RvD1 production in response to LPS.

Trial registration

The project was registered at ClinicalTrial.gov (NCT02177383).
Literature
1.
go back to reference Bassit RA, Curi R, Costa Rosa LF. Creatine supplementation reduces plasma levels of pro-inflammatory cytokines and PGE2 after a half-ironman competition. Amino Acids. 2008;35:425–31.CrossRefPubMed Bassit RA, Curi R, Costa Rosa LF. Creatine supplementation reduces plasma levels of pro-inflammatory cytokines and PGE2 after a half-ironman competition. Amino Acids. 2008;35:425–31.CrossRefPubMed
2.
go back to reference Burd NA, Dickinson JM, Lemoine JK, Carroll CC, Sullivan BE, Haus JM, Jemiolo B, Trappe SW, Hughes GM, Sanders CE, Jr., Trappe TA. Effect of a cyclooxygenase-2 inhibitor on postexercise muscle protein synthesis in humans. Am J Physiol Endocrinol Metab. 2010;298:E354–361.CrossRefPubMedPubMedCentral Burd NA, Dickinson JM, Lemoine JK, Carroll CC, Sullivan BE, Haus JM, Jemiolo B, Trappe SW, Hughes GM, Sanders CE, Jr., Trappe TA. Effect of a cyclooxygenase-2 inhibitor on postexercise muscle protein synthesis in humans. Am J Physiol Endocrinol Metab. 2010;298:E354–361.CrossRefPubMedPubMedCentral
3.
go back to reference Calder PC. Polyunsaturated fatty acids and inflammatory processes: New twists in an old tale. Biochimie. 2009;91:791–5.CrossRefPubMed Calder PC. Polyunsaturated fatty acids and inflammatory processes: New twists in an old tale. Biochimie. 2009;91:791–5.CrossRefPubMed
4.
go back to reference Calder PC, Grimble RF. Polyunsaturated fatty acids, inflammation and immunity. Eur J Clin Nutr. 2002;56 Suppl 3:S14–19.CrossRefPubMed Calder PC, Grimble RF. Polyunsaturated fatty acids, inflammation and immunity. Eur J Clin Nutr. 2002;56 Suppl 3:S14–19.CrossRefPubMed
5.
go back to reference Cannon JG. Inflammatory Cytokines in Nonpathological States. News Physiol Sci. 2000;15:298–303.PubMed Cannon JG. Inflammatory Cytokines in Nonpathological States. News Physiol Sci. 2000;15:298–303.PubMed
6.
go back to reference Capo X, Martorell M, Llompart I, Sureda A, Tur JA, Pons A. Docosahexanoic acid diet supplementation attenuates the peripheral mononuclear cell inflammatory response to exercise following LPS activation. Cytokine. 2014;69:155–64.CrossRefPubMed Capo X, Martorell M, Llompart I, Sureda A, Tur JA, Pons A. Docosahexanoic acid diet supplementation attenuates the peripheral mononuclear cell inflammatory response to exercise following LPS activation. Cytokine. 2014;69:155–64.CrossRefPubMed
7.
go back to reference Capo X, Martorell M, Sureda A, Llompart I, Tur JA, Pons A. Diet supplementation with DHA-enriched food in football players during training season enhances the mitochondrial antioxidant capabilities in blood mononuclear cells. Eur J Nutr. 2015;54(1):35–49.CrossRefPubMed Capo X, Martorell M, Sureda A, Llompart I, Tur JA, Pons A. Diet supplementation with DHA-enriched food in football players during training season enhances the mitochondrial antioxidant capabilities in blood mononuclear cells. Eur J Nutr. 2015;54(1):35–49.CrossRefPubMed
8.
go back to reference Carroll CC, O’Connor DT, Steinmeyer R, Del Mundo JD, McMullan DR, Whitt JA, Ramos JE, Gonzales RJ. The influence of acute resistance exercise on cyclooxygenase-1 and -2 activity and protein levels in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2013;305:R24–30.CrossRefPubMed Carroll CC, O’Connor DT, Steinmeyer R, Del Mundo JD, McMullan DR, Whitt JA, Ramos JE, Gonzales RJ. The influence of acute resistance exercise on cyclooxygenase-1 and -2 activity and protein levels in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2013;305:R24–30.CrossRefPubMed
9.
go back to reference Conceicao MS, Libardi CA, Nogueira FR, Bonganha V, Gaspari AF, Chacon-Mikahil MP, Cavaglieri CR, Madruga VA. Effects of eccentric exercise on systemic concentrations of pro- and anti-inflammatory cytokines and prostaglandin (E2): comparison between young and postmenopausal women. Eur J Appl Physiol. 2012;112:3205–13.CrossRefPubMed Conceicao MS, Libardi CA, Nogueira FR, Bonganha V, Gaspari AF, Chacon-Mikahil MP, Cavaglieri CR, Madruga VA. Effects of eccentric exercise on systemic concentrations of pro- and anti-inflammatory cytokines and prostaglandin (E2): comparison between young and postmenopausal women. Eur J Appl Physiol. 2012;112:3205–13.CrossRefPubMed
10.
go back to reference Chiang N, Fredman G, Backhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature. 2012;484:524–8.CrossRefPubMedPubMedCentral Chiang N, Fredman G, Backhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature. 2012;484:524–8.CrossRefPubMedPubMedCentral
11.
go back to reference Frassdorf J, Luther B, Mullenheim J, Otto F, Preckel B, Schlack W, Thamer V. Influence of groin incision, duration of ischemia, and prostaglandin E1 on ischemia-reperfusion injury of the lower limb. J Cardiothorac Vasc Anesth. 2006;20:187–95.CrossRefPubMed Frassdorf J, Luther B, Mullenheim J, Otto F, Preckel B, Schlack W, Thamer V. Influence of groin incision, duration of ischemia, and prostaglandin E1 on ischemia-reperfusion injury of the lower limb. J Cardiothorac Vasc Anesth. 2006;20:187–95.CrossRefPubMed
12.
go back to reference Gleeson M, McFarlin B, Flynn M. Exercise and Toll-like receptors. Exerc Immunol Rev. 2006;12:34–53.PubMed Gleeson M, McFarlin B, Flynn M. Exercise and Toll-like receptors. Exerc Immunol Rev. 2006;12:34–53.PubMed
13.
go back to reference Hassan A, Ibrahim A, Mbodji K, Coeffier M, Ziegler F, Bounoure F, Chardigny JM, Skiba M, Savoye G, Dechelotte P, Marion-Letellier R. An alpha-linolenic acid-rich formula reduces oxidative stress and inflammation by regulating NF-kappaB in rats with TNBS-induced colitis. J Nutr. 2010;140:1714–21.CrossRefPubMed Hassan A, Ibrahim A, Mbodji K, Coeffier M, Ziegler F, Bounoure F, Chardigny JM, Skiba M, Savoye G, Dechelotte P, Marion-Letellier R. An alpha-linolenic acid-rich formula reduces oxidative stress and inflammation by regulating NF-kappaB in rats with TNBS-induced colitis. J Nutr. 2010;140:1714–21.CrossRefPubMed
14.
go back to reference Helge JW, Ayre KJ, Hulbert AJ, Kiens B, Storlien LH. Regular exercise modulates muscle membrane phospholipid profile in rats. J Nutr. 1999;129:1636–42.PubMed Helge JW, Ayre KJ, Hulbert AJ, Kiens B, Storlien LH. Regular exercise modulates muscle membrane phospholipid profile in rats. J Nutr. 1999;129:1636–42.PubMed
15.
go back to reference Helge JW, Wu BJ, Willer M, Daugaard JR, Storlien LH, Kiens B. Training affects muscle phospholipid fatty acid composition in humans. J Appl Physiol (1985). 2001;90:670–7. Helge JW, Wu BJ, Willer M, Daugaard JR, Storlien LH, Kiens B. Training affects muscle phospholipid fatty acid composition in humans. J Appl Physiol (1985). 2001;90:670–7.
16.
go back to reference Hirose L, Nosaka K, Newton M, Laveder A, Kano M, Peake J, Suzuki K. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev. 2004;10:75–90.PubMed Hirose L, Nosaka K, Newton M, Laveder A, Kano M, Peake J, Suzuki K. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc Immunol Rev. 2004;10:75–90.PubMed
17.
go back to reference Karamouzis M, Karamouzis I, Vamvakoudis E, Ampatzidis G, Christoulas K, Angelopoulou N, Mandroukas K. The response of muscle interstitial prostaglandin E(2)(PGE(2)), prostacyclin I(2)(PGI(2)) and thromboxane A(2)(TXA(2)) levels during incremental dynamic exercise in humans determined by in vivo microdialysis. Prostaglandins Leukot Essent Fat Acids. 2001;64:259–63.CrossRef Karamouzis M, Karamouzis I, Vamvakoudis E, Ampatzidis G, Christoulas K, Angelopoulou N, Mandroukas K. The response of muscle interstitial prostaglandin E(2)(PGE(2)), prostacyclin I(2)(PGI(2)) and thromboxane A(2)(TXA(2)) levels during incremental dynamic exercise in humans determined by in vivo microdialysis. Prostaglandins Leukot Essent Fat Acids. 2001;64:259–63.CrossRef
18.
go back to reference Khalfoun B, Thibault F, Watier H, Bardos P, Lebranchu Y. Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6. Adv Exp Med Biol. 1997;400b:589–97.PubMed Khalfoun B, Thibault F, Watier H, Bardos P, Lebranchu Y. Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6. Adv Exp Med Biol. 1997;400b:589–97.PubMed
19.
go back to reference LaVoy EC, Bosch JA, Lowder TW, Simpson RJ. Acute aerobic exercise in humans increases cytokine expression in CD27(-) but not CD27(+) CD8(+) T-cells. Brain Behav Immun. 2013;27:54–62.CrossRefPubMed LaVoy EC, Bosch JA, Lowder TW, Simpson RJ. Acute aerobic exercise in humans increases cytokine expression in CD27(-) but not CD27(+) CD8(+) T-cells. Brain Behav Immun. 2013;27:54–62.CrossRefPubMed
20.
go back to reference Lee TH, Hoover RL, Williams JD, Sperling RI, Ravalese 3rd J, Spur BW, Robinson DR, Corey EJ, Lewis RA, Austen KF. Effect of dietary enrichment with eicosapentaenoic and docosahexaenoic acids on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N Engl J Med. 1985;312:1217–24.CrossRefPubMed Lee TH, Hoover RL, Williams JD, Sperling RI, Ravalese 3rd J, Spur BW, Robinson DR, Corey EJ, Lewis RA, Austen KF. Effect of dietary enrichment with eicosapentaenoic and docosahexaenoic acids on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N Engl J Med. 1985;312:1217–24.CrossRefPubMed
21.
go back to reference Liu Y, Chen LY, Sokolowska M, Eberlein M, Alsaaty S, Martinez-Anton A, Logun C, Qi HY, Shelhamer JH. The fish oil ingredient, docosahexaenoic acid, activates cytosolic phospholipase A2 via GPR120 receptor to produce prostaglandin E2 and plays an anti-inflammatory role in macrophages. Immunology. 2014;143(1):81–95.CrossRefPubMedPubMedCentral Liu Y, Chen LY, Sokolowska M, Eberlein M, Alsaaty S, Martinez-Anton A, Logun C, Qi HY, Shelhamer JH. The fish oil ingredient, docosahexaenoic acid, activates cytosolic phospholipase A2 via GPR120 receptor to produce prostaglandin E2 and plays an anti-inflammatory role in macrophages. Immunology. 2014;143(1):81–95.CrossRefPubMedPubMedCentral
22.
go back to reference Markworth JF, Vella L, Lingard BS, Tull DL, Rupasinghe TW, Sinclair AJ, Maddipati KR, Cameron-Smith D. Human inflammatory and resolving lipid mediator responses to resistance exercise and ibuprofen treatment. Am J Physiol Regul Integr Comp Physiol. 2013;305:R1281–1296.CrossRefPubMedPubMedCentral Markworth JF, Vella L, Lingard BS, Tull DL, Rupasinghe TW, Sinclair AJ, Maddipati KR, Cameron-Smith D. Human inflammatory and resolving lipid mediator responses to resistance exercise and ibuprofen treatment. Am J Physiol Regul Integr Comp Physiol. 2013;305:R1281–1296.CrossRefPubMedPubMedCentral
23.
go back to reference Martorell M, Capo X, Bibiloni MM, Sureda A, Mestre-Alfaro A, Batle JM, Llompart I, Tur JA, Pons A. Docosahexaenoic Acid Supplementation Promotes Erythrocyte Antioxidant Defense and Reduces Protein Nitrosative Damage in Male Athletes. Lipids. 2015;50(2):131–48.CrossRefPubMed Martorell M, Capo X, Bibiloni MM, Sureda A, Mestre-Alfaro A, Batle JM, Llompart I, Tur JA, Pons A. Docosahexaenoic Acid Supplementation Promotes Erythrocyte Antioxidant Defense and Reduces Protein Nitrosative Damage in Male Athletes. Lipids. 2015;50(2):131–48.CrossRefPubMed
24.
go back to reference Martorell M, Capo X, Sureda A, Tur JA, Pons A. Effects of docosahexaenoic acid diet supplementation, training, and acute exercise on oxidative balance in neutrophils. Appl Physiol Nutr Metab. 2014;39:446–57.CrossRefPubMed Martorell M, Capo X, Sureda A, Tur JA, Pons A. Effects of docosahexaenoic acid diet supplementation, training, and acute exercise on oxidative balance in neutrophils. Appl Physiol Nutr Metab. 2014;39:446–57.CrossRefPubMed
25.
go back to reference Mathur N, Pedersen BK. Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm. 2008;2008:109502.CrossRef Mathur N, Pedersen BK. Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm. 2008;2008:109502.CrossRef
26.
go back to reference Nikolaidis MG, Mougios V. Effects of exercise on the fatty-acid composition of blood and tissue lipids. Sports Medicine (Auckland, NZ). 2004;34:1051–76.CrossRef Nikolaidis MG, Mougios V. Effects of exercise on the fatty-acid composition of blood and tissue lipids. Sports Medicine (Auckland, NZ). 2004;34:1051–76.CrossRef
27.
go back to reference Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18:6853–66.CrossRefPubMed Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18:6853–66.CrossRefPubMed
28.
go back to reference Pedersen BK. Muscle as a secretory organ. Compr Physiol. 2013;3:1337–62.PubMed Pedersen BK. Muscle as a secretory organ. Compr Physiol. 2013;3:1337–62.PubMed
29.
go back to reference Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev. 2000;80:1055–81.PubMed Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev. 2000;80:1055–81.PubMed
30.
go back to reference Rubin D, Laposata M. Regulation of agonist-induced prostaglandin E1 versus prostaglandin E2 production. A mass analysis. J Biol Chem. 1991;266:23618–23.PubMed Rubin D, Laposata M. Regulation of agonist-induced prostaglandin E1 versus prostaglandin E2 production. A mass analysis. J Biol Chem. 1991;266:23618–23.PubMed
31.
go back to reference Schmidt S, Stahl F, Mutz KO, Scheper T, Hahn A, Schuchardt JP. Different gene expression profiles in normo- and dyslipidemic men after fish oil supplementation: results from a randomized controlled trial. Lipids Health Dis. 2012;11:105.CrossRefPubMedPubMedCentral Schmidt S, Stahl F, Mutz KO, Scheper T, Hahn A, Schuchardt JP. Different gene expression profiles in normo- and dyslipidemic men after fish oil supplementation: results from a randomized controlled trial. Lipids Health Dis. 2012;11:105.CrossRefPubMedPubMedCentral
33.
go back to reference Serhan CN, Clish CB, Brannon J, Colgan SP, Gronert K, Chiang N. Anti-microinflammatory lipid signals generated from dietary N-3 fatty acids via cyclooxygenase-2 and transcellular processing: a novel mechanism for NSAID and N-3 PUFA therapeutic actions. J Physiol Pharmacol. 2000;51:643–54.PubMed Serhan CN, Clish CB, Brannon J, Colgan SP, Gronert K, Chiang N. Anti-microinflammatory lipid signals generated from dietary N-3 fatty acids via cyclooxygenase-2 and transcellular processing: a novel mechanism for NSAID and N-3 PUFA therapeutic actions. J Physiol Pharmacol. 2000;51:643–54.PubMed
34.
go back to reference Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025–37.CrossRefPubMedPubMedCentral Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025–37.CrossRefPubMedPubMedCentral
35.
go back to reference Sureda A, Ferrer MD, Tauler P, Romaguera D, Drobnic F, Pujol P, Tur JA, Pons A. Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players. Br J Sports Med. 2009;43:186–90.CrossRefPubMed Sureda A, Ferrer MD, Tauler P, Romaguera D, Drobnic F, Pujol P, Tur JA, Pons A. Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players. Br J Sports Med. 2009;43:186–90.CrossRefPubMed
36.
go back to reference Toft AD, Thorn M, Ostrowski K, Asp S, Moller K, Iversen S, Hermann C, Sondergaard SR, Pedersen BK. N-3 polyunsaturated fatty acids do not affect cytokine response to strenuous exercise. J Appl Physiol (1985). 2000;89:2401–6. Toft AD, Thorn M, Ostrowski K, Asp S, Moller K, Iversen S, Hermann C, Sondergaard SR, Pedersen BK. N-3 polyunsaturated fatty acids do not affect cytokine response to strenuous exercise. J Appl Physiol (1985). 2000;89:2401–6.
37.
go back to reference Trappe TA, Fluckey JD, White F, Lambert CP, Evans WJ. Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J Clin Endocrinol Metab. 2001;86:5067–70.PubMed Trappe TA, Fluckey JD, White F, Lambert CP, Evans WJ. Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J Clin Endocrinol Metab. 2001;86:5067–70.PubMed
38.
go back to reference Trappe TA, Liu SZ. Effects of prostaglandins and COX-inhibiting drugs on skeletal muscle adaptations to exercise. J Appl Physiol (1985). 2013;115:909–19.CrossRefPubMedCentral Trappe TA, Liu SZ. Effects of prostaglandins and COX-inhibiting drugs on skeletal muscle adaptations to exercise. J Appl Physiol (1985). 2013;115:909–19.CrossRefPubMedCentral
39.
go back to reference Uchida MC, Nosaka K, Ugrinowitsch C, Yamashita A, Martins Jr E, Moriscot AS, Aoki MS. Effect of bench press exercise intensity on muscle soreness and inflammatory mediators. J Sports Sci. 2009;27:499–507.CrossRefPubMed Uchida MC, Nosaka K, Ugrinowitsch C, Yamashita A, Martins Jr E, Moriscot AS, Aoki MS. Effect of bench press exercise intensity on muscle soreness and inflammatory mediators. J Sports Sci. 2009;27:499–507.CrossRefPubMed
40.
go back to reference Volek JS, Rawson ES. Scientific basis and practical aspects of creatine supplementation for athletes. Nutrition (Burbank, Los Angeles County, Calif). 2004;20:609–14.CrossRef Volek JS, Rawson ES. Scientific basis and practical aspects of creatine supplementation for athletes. Nutrition (Burbank, Los Angeles County, Calif). 2004;20:609–14.CrossRef
41.
go back to reference Weiss T, Eckstein H, Weiss C, Diehm C. Neutrophil function in peripheral arterial occlusive disease: the effects of prostaglandin E1. Vascular medicine (London, England). 1998;3:171–5.CrossRef Weiss T, Eckstein H, Weiss C, Diehm C. Neutrophil function in peripheral arterial occlusive disease: the effects of prostaglandin E1. Vascular medicine (London, England). 1998;3:171–5.CrossRef
Metadata
Title
Effects of dietary Docosahexaenoic, training and acute exercise on lipid mediators
Authors
X. Capó
M. Martorell
A. Sureda
J. A. Tur
A. Pons
Publication date
01-12-2016
Publisher
BioMed Central
DOI
https://doi.org/10.1186/s12970-016-0126-y

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