Advertisement

European Journal of Nutrition

, Volume 54, Issue 1, pp 35–49 | Cite as

Diet supplementation with DHA-enriched food in football players during training season enhances the mitochondrial antioxidant capabilities in blood mononuclear cells

  • Xavier Capó
  • Miquel Martorell
  • Antoni Sureda
  • Isabel Llompart
  • Josep A. Tur
  • Antoni PonsEmail author
Original Contribution

Abstract

Purpose

Exercise induces oxidative stress and causes adaptations in antioxidant defenses. The aim of the present study was to determine the effects of a 2-month diet supplementation with docosahexaenoic acid (DHA) on the pro-oxidant and antioxidant status of peripheral blood mononuclear cells (PBMCs) during football training and after acute exercise.

Methods

Fifteen male football players, in a randomized double-blind trial, ingested a beverage enriched with DHA or a placebo for 8 weeks. Blood samples were collected in basal conditions before and after the training period and after an acute and intense exercise.

Results

The training season increased the carbonyl and nitrotyrosine index but decreased the malondialdehyde (MDA) levels. Basal catalase activity decreased in both groups after 8 weeks of training, whereas glutathione peroxidase activity increased mainly in the placebo group. Protein levels of uncoupling proteins (UCP2 and UCP3) and inducible nitric oxide synthase significantly increased after the training period. Acute exercise induced redistribution in the number of circulating cells, increased the MDA levels and nitrotyrosine index, and decreased the levels of nitrate. Acute exercise also increased PBMCs reactive oxygen species (ROS) production after immune stimulation. Diet supplementation with DHA significantly increased the UCP3 levels after training and the superoxide dismutase protein levels after acute exercise, and reduced the production of ROS after acute exercise.

Conclusion

Docosahexaenoic acid increased the antioxidant capabilities while reducing the mitochondrial ROS production in a regular football training period and reduced the oxidative damage markers in response to acute exercise.

Keywords

DHA PBMC Oxidative stress Exercise ROS production 

Notes

Acknowledgments

Acción Estratégica en Salud del Ministro de Ciencia e Innovación DPS2008-07033-C03-03, Programme of Promotion of Biomedical Research and Health Sciences, Projects 11/01791, Red Predimed-RETIC RD06/0045/1004, CIBERobn CB12/03/30038 and Balearic Island Government and FEDER funds (35/2011 and 23/2012). We would like to thank the football players involved in the study for their committed participation. The excellent technical and practical assistance of Tomeu Munar, Cédric Thyus and RCD Mallorca is appreciated.

Conflict of interest

The authors declare that they do not have any conflict of interest.

References

  1. 1.
    Costill DL, Wilmore JH (2004) Fisiología del esfuerzo y del deporte. Paidotribo, BarcelonaGoogle Scholar
  2. 2.
    Ji LL (1995) Oxidative stress during exercise: implication of antioxidant nutrients. Free Radic Biol Med 18:1079–1086CrossRefGoogle Scholar
  3. 3.
    Radak Z, Zhao Z, Koltai E, Ohno H, Atalay M (2013) Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid Redox Signal 18:1208–1246. doi: 10.1089/ars.2011.4498 CrossRefGoogle Scholar
  4. 4.
    Viña J, Gimeno A, Sastre J, Desco C, Asensi M, Pallardó FV, Cuesta A, Ferrero JA, Terada LS, Repine JE (2000) Mechanism of free radical production in exhaustive exercise in humans and rats; role of xanthine oxidase and protection by allopurinol. IUBMB Life 49:539–544. doi: 10.1080/15216540050167098 CrossRefGoogle Scholar
  5. 5.
    Sureda A, Batle JM, Ferrer MD, Mestre-Alfaro A, Tur JA, Pons A (2012) Scuba diving activates vascular antioxidant system. Int J Sports Med 33:531–536. doi: 10.1055/s-0031-1297957 CrossRefGoogle Scholar
  6. 6.
    Wagner KH, Reichhold S, Neubauer O (2011) Impact of endurance and ultraendurance exercise on DNA damage. Ann N Y Acad Sci 1229:115–123. doi: 10.1111/j.1749-6632.2011.06106.x CrossRefGoogle Scholar
  7. 7.
    Nikolaidis MG, Jamurtas AZ (2009) Blood as a reactive species generator and redox status regulator during exercise. Arch Biochem Biophys 490:77–84. doi: 10.1016/j.abb.2009.08.015 CrossRefGoogle Scholar
  8. 8.
    Ferrer MD, Sureda A, Mestre A, Tur JA, Pons A (2010) The double edge of reactive oxygen species as damaging and signaling molecules in HL60 cell culture. Cell Physiol Biochem 25:241–252. doi: 10.1159/000276558 CrossRefGoogle Scholar
  9. 9.
    Alessio HM, Goldfarb AH (1988) Lipid peroxidation and scavenger enzymes during exercise: adaptive response to training. J Appl Physiol 64:1333–1336Google Scholar
  10. 10.
    Korzeniowska-Kubacka I, Bilińska M, Piotrowicz R (2007) Influence of physical training on cardiac performance in patients with coronary artery disease and exercise-induced left ventricular dysfunction. Acta Cardiol 62:573–578CrossRefGoogle Scholar
  11. 11.
    Nicks CR, Morgan DW, Fuller DK, Caputo JL (2009) The influence of respiratory muscle training upon intermittent exercise performance. Int J Sports Med 30:16–21. doi: 10.1055/s-2008-1038794 CrossRefGoogle Scholar
  12. 12.
    Tian Y, Nie J, Tong TK, Baker JS, Thomas NE, Shi Q (2010) Serum oxidant and antioxidant status during early and late recovery periods following an all-out 21-km run in trained adolescent runners. Eur J Appl Physiol 110:971–976. doi: 10.1007/s00421-010-1583-7 CrossRefGoogle Scholar
  13. 13.
    Cases N, Aguiló A, Tauler P, Sureda A, Llompart I, Pons A, Tur JA (2005) Differential response of plasma and immune cell’s vitamin E levels to physical activity and antioxidant vitamin supplementation. Eur J Clin Nutr 59:781–788. doi: 10.1038/sj.ejcn.1602143 CrossRefGoogle Scholar
  14. 14.
    Vina J, Borras C, Gomez-Cabrera MC, Orr WC (2006) Part of the series: from dietary antioxidants to regulators in cellular signalling and gene expression. Role of reactive oxygen species and (phyto)oestrogens in the modulation of adaptive response to stress. Free Radic Res 40:111–119. doi: 10.1080/10715760500405778 CrossRefGoogle Scholar
  15. 15.
    Sureda A, Tauler P, Aguiló A, Fuentespina E, Córdova A, Tur JA, Pons A (2006) Blood cell NO synthesis in response to exercise. Nitric Oxide 15:5–12. doi: 10.1016/j.niox.2005.11.004 CrossRefGoogle Scholar
  16. 16.
    Tauler P, Sureda A, Cases N, Aguiló A, Rodríguez-Marroyo JA, Villa G, Tur JA, Pons A (2006) Increased lymphocyte antioxidant defences in response to exhaustive exercise do not prevent oxidative damage. J Nutr Biochem 17:665–671. doi: 10.1016/j.jnutbio.2005.10.013 CrossRefGoogle Scholar
  17. 17.
    Ferrer MD, Sureda A, Batle JM, Tauler P, Tur JA, Pons A (2007) Scuba diving enhances endogenous antioxidant defenses in lymphocytes and neutrophils. Free Radic Res 41:274–281. doi: 10.1080/10715760601080371 CrossRefGoogle Scholar
  18. 18.
    Cortright RN, Zheng D, Jones JP, Fluckey JD, DiCarlo SE, Grujic D, Lowell BB, Dohm GL (1999) Regulation of skeletal muscle UCP-2 and UCP-3 gene expression by exercise and denervation. Am J Physiol 276:E217–E221Google Scholar
  19. 19.
    Sureda A, Tauler P, Aguiló A, Cases N, Llompart I, Tur JA, Pons A (2008) Influence of an antioxidant vitamin-enriched drink on pre- and post-exercise lymphocyte antioxidant system. Ann Nutr Metab 52:233–240. doi: 10.1159/000140515 CrossRefGoogle Scholar
  20. 20.
    Uauy-Dagach R, Mena P, Hoffman DR (1994) Essential fatty acid metabolism and requirements for LBW infants. Acta Paediatr Suppl 405:78–85CrossRefGoogle Scholar
  21. 21.
    Maki KC, Van Elswyk ME, McCarthy D, Hess SP, Veith PE, Bell M, Subbaiah P, Davidson MH (2005) Lipid responses to a dietary docosahexaenoic acid supplement in men and women with below average levels of high density lipoprotein cholesterol. J Am Coll Nutr 24:189–199CrossRefGoogle Scholar
  22. 22.
    Crawford MA (2006) Docosahexaenoic acid in neural signaling systems. Nutr Health 18:263–276CrossRefGoogle Scholar
  23. 23.
    Innis SM (2007) Dietary (n-3) fatty acids and brain development. J Nutr 137:855–859Google Scholar
  24. 24.
    Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, Saito Y, Ishikawa Y, Oikawa S, Sasaki J, Hishida H, Itakura H, Kita T, Kitabatake A, Nakaya N, Sakata T, Shimada K, Shirato K, Investigators JElisJ (2007) Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised open-label, blinded endpoint analysis. Lancet 369:1090–1098Google Scholar
  25. 25.
    Mori TA, Codde JP, Vandongen R, Beilin LJ (1987) New findings in the fatty acid composition of individual platelet phospholipids in man after dietary fish oil supplementation. Lipids 22:744–750CrossRefGoogle Scholar
  26. 26.
    Dawczynski C, Hackermeier U, Viehweger M, Stange R, Springer M, Jahreis G (2011) Incorporation of n-3 PUFA and γ-linolenic acid in blood lipids and red blood cell lipids together with their influence on disease activity in patients with chronic inflammatory arthritis–a randomized controlled human intervention trial. Lipids Health Dis 10:130. doi: 10.1186/1476-511X-10-130 CrossRefGoogle Scholar
  27. 27.
    Tur JA, Bibiloni MM, Sureda A, Pons A (2012) Dietary sources of omega 3 fatty acids: public health risks and benefits. Br J Nutr 107(Suppl 2):S23–S52. doi: 10.1017/S0007114512001456 CrossRefGoogle Scholar
  28. 28.
    Tartibian B, Maleki BH, Abbasi A (2011) Omega-3 fatty acids supplementation attenuates inflammatory markers after eccentric exercise in untrained men. Clin J Sport Med 21:131–137. doi: 10.1097/JSM.0b013e31820f8c2f CrossRefGoogle Scholar
  29. 29.
    Lorente-Cebrián S, Bustos M, Marti A, Martinez JA, Moreno-Aliaga MJ (2009) Eicosapentaenoic acid stimulates AMP-activated protein kinase and increases visfatin secretion in cultured murine adipocytes. Clin Sci 117:243–249. doi: 10.1042/CS20090020 CrossRefGoogle Scholar
  30. 30.
    Motawi TM, Hashem RM, Rashed LA, El-Razek SM (2009) Comparative study between the effect of the peroxisome proliferator activated receptor-alpha ligands fenofibrate and n-3 polyunsaturated fatty acids on activation of 5′-AMP-activated protein kinase-alpha1 in high-fat fed rats. J Pharm Pharmacol 61:1339–1346. doi: 10.1211/jpp/61.10.0010 CrossRefGoogle Scholar
  31. 31.
    Siddiqui RA, Harvey K, Stillwell W (2008) Anticancer properties of oxidation products of docosahexaenoic acid. Chem Phys Lipids 153:47–56. doi: 10.1016/j.chemphyslip.2008.02.009 CrossRefGoogle Scholar
  32. 32.
    Filaire E, Massart A, Portier H, Rouveix M, Rosado F, Bage AS, Gobert M, Durand D (2010) Effect of 6 Weeks of n-3 fatty-acid supplementation on oxidative stress in Judo athletes. Int J Sport Nutr Exerc Metab 20:496–506Google Scholar
  33. 33.
    Richard D, Kefi K, Barbe U, Bausero P, Visioli F (2008) Polyunsaturated fatty acids as antioxidants. Pharmacol Res 57:451–455. doi: 10.1016/j.phrs.2008.05.002 CrossRefGoogle Scholar
  34. 34.
    Di Nunzio M, Valli V, Bordoni A (2011) Pro- and anti-oxidant effects of polyunsaturated fatty acid supplementation in HepG2 cells. Prostaglandins Leukot Essent Fatty Acids 85:121–127. doi: 10.1016/j.plefa.2011.07.005 CrossRefGoogle Scholar
  35. 35.
    Tholstrup T, Hellgren LI, Petersen M, Basu S, Straarup EM, Schnohr P, Sandström B (2004) A solid dietary fat containing fish oil redistributes lipoprotein subclasses without increasing oxidative stress in men. J Nutr 134:1051–1057Google Scholar
  36. 36.
    Sureda A, Ferrer MD, Tauler P, Romaguera D, Drobnic F, Pujol P, Tur JA, Pons A (2009) Effects of exercise intensity on lymphocyte H2O2 production and antioxidant defences in soccer players. Br J Sports Med 43:186–190CrossRefGoogle Scholar
  37. 37.
    Mack GW, Yang R, Hargens AR, Nagashima K, Haskell A (1998) Influence of hydrostatic pressure gradients on regulation of plasma volume after exercise. J Appl Physiol 85:667–675Google Scholar
  38. 38.
    Tauler P, Ferrer MD, Romaguera D, Sureda A, Aguilo A, Tur J, Pons A (2008) Antioxidant response and oxidative damage induced by a swimming session: influence of gender. J Sports Sci 26:1303–1311. doi: 10.1080/02640410801974992 CrossRefGoogle Scholar
  39. 39.
    Boyum A (1964) Separation of white blood cells. Nature 204:793–794CrossRefGoogle Scholar
  40. 40.
    Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509Google Scholar
  41. 41.
    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 72:248–254CrossRefGoogle Scholar
  42. 42.
    Braman RS, Hendrix SA (1989) Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal Chem 61:2715–2718CrossRefGoogle Scholar
  43. 43.
    Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  44. 44.
    Goldberg DM Spooner R (1984) Glutathione reductase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Enzymes 1: oxidoreductases, transferases, vol 3. Verlag chemie, Basel, pp 258–265Google Scholar
  45. 45.
    Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121CrossRefGoogle Scholar
  46. 46.
    Toft AD, Thorn M, Ostrowski K, Asp S, Moller K, Iversen S, Hermann C, Sondergaard SR, Pedersen BK (2000) N-3 polyunsaturated fatty acids do not affect cytokine response to strenuous exercise. J Appl Physiol 89:2401–2406Google Scholar
  47. 47.
    Ferrer MD, Tauler P, Sureda A, Pujol P, Drobnic F, Tur JA, Pons A (2009) A soccer match’s ability to enhance lymphocyte capability to produce ROS and induce oxidative damage. Int J Sport Nutr Exerc Metab 19:243–258Google Scholar
  48. 48.
    Blough N, Zafkiou O (1985) Reaction of superoxide with nitric oxide to form peroxonitrite in alkaline aqueous solution. Inorg Chem 24:3502–3504CrossRefGoogle Scholar
  49. 49.
    Radi R, Beckman JS, Bush KM, Freeman BA (1991) Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 288:481–487CrossRefGoogle Scholar
  50. 50.
    Radi R, Beckman JS, Bush KM, Freeman BA (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 266:4244–4250Google Scholar
  51. 51.
    Moreno JJ, Pryor WA (1992) Inactivation of alpha 1-proteinase inhibitor by peroxynitrite. Chem Res Toxicol 5:425–431CrossRefGoogle Scholar
  52. 52.
    Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620–1624CrossRefGoogle Scholar
  53. 53.
    Kastle M, Grune T (2011) Protein oxidative modification in the aging organism and the role of the ubiquitin proteasomal system. Curr Pharm Des 17:4007–4022CrossRefGoogle Scholar
  54. 54.
    Miyata T, Inagi R, Asahi K, Yamada Y, Horie K, Sakai H, Uchida K, Kurokawa K (1998) Generation of protein carbonyls by glycoxidation and lipoxidation reactions with autoxidation products of ascorbic acid and polyunsaturated fatty acids. FEBS Lett 437:24–28CrossRefGoogle Scholar
  55. 55.
    Ferrer MD, Tauler P, Sureda A, Tur JA, Pons A (2009) Antioxidant regulatory mechanisms in neutrophils and lymphocytes after intense exercise. J Sports Sci 27:49–58. doi: 10.1080/02640410802409683 CrossRefGoogle Scholar
  56. 56.
    Siess H (1985) Oxidative stress. Academic Press, LondonGoogle Scholar
  57. 57.
    Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415:96–99. doi: 10.1038/415096a CrossRefGoogle Scholar
  58. 58.
    Cannon B, Shabalina IG, Kramarova TV, Petrovic N, Nedergaard J (2006) Uncoupling proteins: a role in protection against reactive oxygen species—or not? Biochim Biophys Acta 1757:449–458. doi: 10.1016/j.bbabio.2006.05.016 CrossRefGoogle Scholar
  59. 59.
    Jiang N, Zhang G, Bo H, Qu J, Ma G, Cao D, Wen L, Liu S, Ji LL, Zhang Y (2009) Upregulation of uncoupling protein-3 in skeletal muscle during exercise: a potential antioxidant function. Free Radic Biol Med 46:138–145. doi: 10.1016/j.freeradbiomed.2008.09.026 CrossRefGoogle Scholar
  60. 60.
    Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35:505–513. doi: 10.1016/j.tibs.2010.04.002 CrossRefGoogle Scholar
  61. 61.
    Tauler P, Aguiló A, Gimeno I, Noguera A, Agustí A, Tur JA, Pons A (2003) Differential response of lymphocytes and neutrophils to high intensity physical activity and to vitamin C diet supplementation. Free Radic Res 37:931–938CrossRefGoogle Scholar
  62. 62.
    Okutsu M, Suzuki K, Ishijima T, Peake J, Higuchi M (2008) The effects of acute exercise-induced cortisol on CCR2 expression on human monocytes. Brain Behav Immun 22:1066–1071. doi: 10.1016/j.bbi.2008.03.006 CrossRefGoogle Scholar
  63. 63.
    Zararsiz I, Sonmez MF, Yilmaz HR, Tas U, Kus I, Kavakli A, Sarsilmaz M (2006) Effects of omega-3 essential fatty acids against formaldehyde-induced nephropathy in rats. Toxicol Ind Health 22:223–229CrossRefGoogle Scholar
  64. 64.
    Kesavulu MM, Kameswararao B, Apparao C, Kumar EG, Harinarayan CV (2002) Effect of omega-3 fatty acids on lipid peroxidation and antioxidant enzyme status in type 2 diabetic patients. Diabetes Metab 28:20–26Google Scholar
  65. 65.
    Sureda A, Tauler P, Aguiló A, Cases N, Fuentespina E, Córdova A, Tur JA, Pons A (2005) Relation between oxidative stress markers and antioxidant endogenous defences during exhaustive exercise. Free Radic Res 39:1317–1324. doi: 10.1080/10715760500177500 CrossRefGoogle Scholar
  66. 66.
    Sureda A, Ferrer MD, Mestre A, Tur JA, Pons A (2013) Prevention of neutrophil protein oxidation with vitamins C and e diet supplementation without affecting the adaptive response to exercise. Int J Sport Nutr Exerc Metab 23:31–39Google Scholar
  67. 67.
    Bescós R, Rodríguez FA, Iglesias X, Ferrer MD, Iborra E, Pons A (2011) Acute administration of inorganic nitrate reduces VO(2peak) in endurance athletes. Med Sci Sports Exerc 43:1979–1986. doi: 10.1249/MSS.0b013e318217d439 CrossRefGoogle Scholar
  68. 68.
    Tauler P, Aguiló A, Guix P, Jiménez F, Villa G, Tur JA, Córdova A, Pons A (2005) Pre-exercise antioxidant enzyme activities determine the antioxidant enzyme erythrocyte response to exercise. J Sports Sci 23:5–13. doi: 10.1080/02640410410001716724 CrossRefGoogle Scholar
  69. 69.
    Mestre-Alfaro A, Ferrer MD, Sureda A, Tauler P, Martínez E, Bibiloni MM, Micol V, Tur JA, Pons A (2011) Phytoestrogens enhance antioxidant enzymes after swimming exercise and modulate sex hormone plasma levels in female swimmers. Eur J Appl Physiol 111:2281–2294. doi: 10.1007/s00421-011-1862-y CrossRefGoogle Scholar
  70. 70.
    Carrera-Quintanar L, Funes L, Viudes E, Tur J, Micol V, Roche E, Pons A (2012) Antioxidant effect of lemon verbena extracts in lymphocytes of university students performing aerobic training program. Scand J Med Sci Sports 22:454–461. doi: 10.1111/j.1600-0838.2010.01244.x CrossRefGoogle Scholar
  71. 71.
    Wang P, Wu Y, Li X, Ma X, Zhong L (2013) Thioredoxin and thioredoxin reductase control tissue factor activity by thiol redox-dependent mechanism. J Biol Chem 288:3346–3358. doi: 10.1074/jbc.M112.418046 CrossRefGoogle Scholar
  72. 72.
    Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054. doi: 10.1126/science.1158265 CrossRefGoogle Scholar
  73. 73.
    Sureda A, Ferrer MD, Tauler P, Tur JA, Pons A (2008) Lymphocyte antioxidant response and H2O2 production after a swimming session: gender differences. Free Radic Res 42:312–319. doi: 10.1080/10715760801989926 CrossRefGoogle Scholar
  74. 74.
    Phillips MD, Flynn MG, McFarlin BK, Stewart LK, Timmerman KL, Ji H (2008) Resistive exercise blunts LPS-stimulated TNF-alpha and Il-1 beta. Int J Sports Med 29:102–109. doi: 10.1055/s-2007-965115 CrossRefGoogle Scholar
  75. 75.
    Starkie RL, Rolland J, Angus DJ, Anderson MJ, Febbraio MA (2001) Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-alpha levels after prolonged running. Am J Physiol Cell Physiol 280:C769–C774Google Scholar
  76. 76.
    Cha SH, Fukushima A, Sakuma K, Kagawa Y (2001) Chronic docosahexaenoic acid intake enhances expression of the gene for uncoupling protein 3 and affects pleiotropic mRNA levels in skeletal muscle of aged C57BL/6NJcl mice. J Nutr 131:2636–2642Google Scholar
  77. 77.
    Müller JM, Ziegler-Heitbrock HW, Baeuerle PA (1993) Nuclear factor kappa B, a mediator of lipopolysaccharide effects. Immunobiology 187:233–256. doi: 10.1016/S0171-2985(11)80342-6 CrossRefGoogle Scholar
  78. 78.
    Emre Y, Hurtaud C, Nübel T, Criscuolo F, Ricquier D, Cassard-Doulcier AM (2007) Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem J 402:271–278. doi: 10.1042/BJ20061430 CrossRefGoogle Scholar
  79. 79.
    Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E (2004) Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172:2522–2529CrossRefGoogle Scholar
  80. 80.
    Baillie RA, Takada R, Nakamura M, Clarke SD (1999) Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostaglandins Leukot Essent Fatty Acids 60:351–356CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Xavier Capó
    • 1
    • 2
  • Miquel Martorell
    • 1
    • 2
  • Antoni Sureda
    • 1
    • 2
  • Isabel Llompart
    • 1
    • 2
  • Josep A. Tur
    • 1
    • 2
  • Antoni Pons
    • 1
    • 2
    Email author
  1. 1.Laboratory of Physical Activity Sciences, Community Nutrition & Oxidative Stress GroupUniversity of the Balearic IslandsPalma de MallorcaSpain
  2. 2.CIBER: CB12/03/30038, Fisiopatología de la Obesidad y la Nutrición, CIBERobnInstituto de Salud Carlos III (ISCIII)Palma de MallorcaSpain

Personalised recommendations