Abstract
Previous studies have reported that chronic supplementation with shark liver oil (SLO) improves immune response of lymphocyte, macrophage and neutrophil in animal models and humans. In a similar manner, exercise training also stimulates the immune system. However, we are not aware of any study about the association of exercise and SLO supplementation on immune response. Thus, our main goal was to investigate the effect of chronic supplementation with SLO on immune responses of exercise-trained rats. Male Wistar rats were divided into four groups: sedentary with no supplementation (SED, n = 20), sedentary with SLO supplementation (SEDslo, n = 20), exercised (EX, n = 17) and exercised supplemented with SLO (EXslo, n = 19). Rats swam for 6 weeks, 1.5 h/day, in water at 32 ± 1°C, with a load of 6.0% body weight attached to the thorax of rat. Animals were killed 48 h after the last exercise session. SLO supplementation did not change phagocytosis, lysosomal volume, superoxide anion and hydrogen peroxide production by peritoneal macrophages and blood neutrophils. Thymus and spleen lymphocyte proliferation were significantly higher in SEDslo, EX, and EXslo groups compared with SED group (P < 0.05). Gut-associated lymphocyte proliferation, on the other hand, was similar between the four experimental groups. Our findings show that SLO and EX indeed are able to increase lymphocyte proliferation, but their association did not induce further stimulation in the adaptive immune response and also did not modify innate immunity.
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References
Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Ann Rev Immunol 2:283–318. doi:10.1146/annurev.iy.02.040184.001435
Bacurau AV, Belmonte MA, Navarro F, Moraes MR, Pontes FL Jr, Pesquero JL, Araújo RC, Bacurau RF (2007) Effect of a high-intensity exercise training on the metabolism and function of macrophages and lymphocytes of walker 256 tumor bearing rats. Exp Biol Med (Maywood) 232:1289–1299. doi:10.3181/0704-RM-93
Berdel WF (1987) Ether lipids and analogs in experimental cancer therapy: a brief review of the Munich experience. Lipids 22:970–973. doi:10.1007/BF02535567
Bonatto S, Folador A, Aikawa J, Yamazaki R, Pizatto N, Oliveira H, Vecchi R, Curi R, Calder PC, Fernandes LC (2004) Lifelong exposure to dietary fish oil alters macrophage responses in Walker 256 tumor-bearing rats. Cell Imunol 231:56–62. doi:10.1016/j.cellimm.2004.12.001
Brohult A, Brohult J, Brohult S (1972) Effect of irradiation and alkoxyglycerol treatment on the formation of antibodies after Salmonella vaccination. Experientia 28:954–955. doi:10.1007/BF01924969
Calder PC (2001) Polyunsaturated fatty acids, inflammation and immunity. Lipids 36:1007–1024. doi:10.1007/s11745-001-0812-7
Calder PC, Yaqoob P, Thies F, Wallace FA, Miles EA (2002) Fatty acids and lymphocyte functions. Br J Nutr 87:S31–S48. doi:10.1079/BJN2001455
Cheminade C, Gautier V, Hichami A, Allaume P, Le Lannou D, Legrand AB (2002) 1-O-alkylglycerols improve boar sperm motility and fertility. Biol Reprod 66:421–428
Dulisch I, Neumann HA, Lohr GR, Andreesen R (1985) Clonogenicity of normal and malignant hematopoietic progenitor cells after exposure to synthetic alkyl-lymphospholipids. Blut 51:393–399
Ferry A, Rieu P, Laziri F, Guezennec CY, Elhabazi A, Le Page C, Rieu M (1991) Immunomodulations of thymocytes and splenocytes in trained rats. J Appl Physiol 71:815–820
Folch J, Lees M, Stanley GHS (1957) A simple method for isolation and purification of total lipid from animal tissue. J Biol Chem 226:497–509
Hackney AC (2006) Exercise as a stressor to the human neuroendocrine system. Medicina (Kaunas) 42:788–797
Hajimoradi M, Hassan ZM, Pourfathollah AA, Daneshmandi S, Pakravan N (2009) The effect of shark liver oil on the tumor infiltrating lymphocytes and cytokine pattern in mice. J Ethnopharmacol 126(3):565–570
Hallgren B, Larsson S (1962) The glyceryl ethers in man and cow. J Lipid Res 3:39–43
Hill AM, Worthley C, Murphy KJ, Buckley JD, Ferrante A, Howe PRC (2007) n-3 Fatty acid supplementation and regular moderate exercise: differential effects of a combined intervention on neutrophil function. Br J Nutr 98:300–309. doi:10.1017/S0007114507707286
Hoffman-Goetz L, Thorne R, Simpson JA, Arumugan Y (1989) Exercise stress alters murine lymphocyte subset distribution in spleen, lymph nodes and thymus. Clin Exp Immunol 76:307–310
Homma S, Yamamoto N (1990) Activation process of macrophages after in vitro treatment of mouse lymphocyte with dodecylglycerol. Clin Exp Immunol 79:307–313
Krotkiewski M, Przybyszewska M, Janik P (2003) Cytostatic and cytotoxic effects of alkylglycerols (Ecomer). Med Sci Monit 9:PI131–PI135
Kwak YS (2006) Effects of training on spleen and peritoneal exudates reactive oxygen species and lymphocyte proliferation by splenocytes at rest and after an acute bout of exercise. J Sports Sci 24:973–978. doi:10.1080/02640410500386233
Leandro CG, de Lima TM, Alba-Loureiro TC, do Nascimento E, Manhaes de Castro R, de Castro CM, Pithon-Curi TC, Curi R (2007) Stress-induced downregulation of macrophage phagocytic function is attenuated by exercise training in rats. Neuroimmunomodulation 14:4–7. doi:10.1159/000107282
Levada-Pires AC, Lambertucci RH, Mohamad M, Hirabara SM, Curi R, Pithon-Curi TC (2007) Exercise training raises expression of the cytosolic components of NADPH oxidase in rat neutrophils. Eur J Appl Physiol 100:153–160. doi:10.1007/s00421-007-0414-y
Lewkowicz P, Banasik M, Glowacka E, Lewkowicz N, Tchorzewski H (2005) Effect of high doses of shark liver oil supplementation on T cell polarization and peripheral blood polymorphonuclear cell function. Pol Merkur Lekarski 18:686–692
Meksawan K, Venkatraman JT, Awad AB, Pendergast DR (2004) Effect of dietary fat intake and exercise on inflammatory mediators of the immune system in sedentary men and women. J Am Coll Nutr 23:331–340
Moura IMW, Dos Santos FF, Moura JAA, Curi R, Fernandes LC (2002) Creatine supplementation induces alteration in cross-sectional area in skeletal muscle fibers of Wistar rats after swimming training. J Sports Sci Med 3:87–95
Nguyen HX, Tidball JG (2003) Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J Physiol 547:125–132. doi:10.1113/jphysiol.2002.031450
Nieman DC (1994) Exercise, infection, and immunity. Int J Sports Med 15:S131–S141. doi:10.1055/s-2007-1021128
Nieman DC (1997) Exercise immunology: practical applications. Int J Sports Med 18:S91–S100. doi:10.1055/s-2007-972705
Nunes EA, Bonatto S, Oliveira HHP, Rivera NLM, Maiorka A, Krabbe EL, Tanhoffer RA, Fernandes LC (2008) The effect IF dietary supplementation with 9-cis:12-trans and 10-trans:12-cis conjugated linoleic acid (CLA) for nine months on serum cholesterol, lymphocyte proliferation and polymorphonuclear cells function in Beagle dogs. Res Vet Sci 84:62–67. doi:10.1016/j.rvsc.2007.03.010
Palmblad J, Samuelson J, Brohult J (1990) Interactions between alkylglycerols and human neutrophil granulocytes. Scand J Clin Lab Invest 50:363–370. doi:10.3109/00365519009091592
Pedersen BK, Toft AD (2000) Effects of exercise on lymphocytes and cytokines. Br J Sports Med 34:246–251. doi:10.1136/bjsm.34.4.246
Pedrono F, Martin B, Leduc C, Le Lan J, Saiag B, Legrand P, Moulinoux JP, Legrand AB (2004a) Natural alkylglycerols restrain growth and metastasis of grafted tumors in mice. Nutr Cancer 48:64–69. doi:10.1207/s15327914nc4801_9
Pedrono F, Khan NA, Legrand AB (2004b) Regulation of calcium signalling by 1-O-alkylglycerols in human Jurkat T lymphocytes. Life Sci 74:2793–2801. doi:10.1016/j.lfs.2003.11.002
Peijie C, Hongwu L, Fengpeng X, Jie R, Jie Z (2003) Heavy load exercise induced dysfunction of immunity and neuroendocrine responses in rats. Life Sci 4:2255–2262. doi:10.1016/S0024-3205(03)00115-2
Pick E, Mizel M (1981) Rapid microassay for the measurement of superoxide and hydrogen peroxide production by macrophages in culture an automatic enzyme immunoassay reader. J Immunol Methods 46:211–226
Pithon-Curi TC, Schumacher RI, Freitas JJS, Lagranha C, Newsholme P, Palanch AC, Doi SQ, Curi R (2003) Glutamine delays spontaneous apoptosis in neutrophils. Am J Physiol 284:1355–1361. doi:10.1152/ajpcell.00224.2002
Pizatto N, Bonatto S, Piconcelli M, Souza LM, Sassaki GL, Naliwaiko K, Nunes EA, Curi R, Calder PC, Fernandes LC (2006) Fish oil alters T-lymphocyte proliferation and macrophage responses in Walker 256 tumor-bearing rats. Nutrition 22:425–432. doi:10.1016/j.nut.2005.11.001
Pugliese PT, Jordan K, Cederberg H, Brohult J (1998) Some biological actions of alkylglycerols from shark liver oil. J Altern Complement Med 4:87–99. doi:10.1089/acm.1998.4.1-87
Rombaldi AJ (1996) Some biochemistry effects of liquid carbohydrate ingested on intermittent high-intensity exercise performance in rats. Doctoral thesis, Federal University of Santa Maria, Rio Grande do Sul, Brazil
Santos RVT, Caperuto EC, Costa Rosa LFBP (2007) Effects of acute exhaustive physical exercise upon glutamine metabolism of lymphocytes from trained rats. Life Sci 80:573–578. doi:10.1016/j.lfs.2006.10.015
Sassaki GL, Souza LM, Serrato RV, Cipriani TR, Gorin PAJ, Iacomini M (2008) Application of acetate derivatives for gas chromatography-mass spectrometry: novel approaches on carbohydrates, lipids and amino acids analysis. J Chromatrogr 1208:215–222
Sugiura H, Nishida H, Inaba R, Mirbod SM, Iwata H (2001) Effects of different durations of exercise on macrophage functions in mice. J Appl Physiol 90:789–794
Tharp GD, Preuss TL (1991) Mitogenic response of T-lymphocytes to exercise training and stress. J Appl Physiol 70:2535–2538
Yamamoto N, Ngwenya BZ (1987) Activation of mouse peritoneal macrophages by lysophospholipids and ether derivatives of neutral lipids and phospholipids. Cancer Res 47:2008–2013
Yamamoto N, St Claire DA, Homma S, Ngwenya BZ (1988) Activation of mouse macrophages by alkylglycerols, inflammation products of cancerous tissues. Cancer Res 48:6044–6049
Acknowledgments
The authors would like to thank Araceli Goedert and Kleverton Krinski for their assistance during experimental trials. This study was supported by Pronex-CNPq, CAPES, and Fundação Araucária.
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Communicated by William Kraemer.
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Vitorino, D.C., Buzzachera, C.F., Curi, R. et al. Effect of chronic supplementation with shark liver oil on immune responses of exercise-trained rats. Eur J Appl Physiol 108, 1225–1232 (2010). https://doi.org/10.1007/s00421-009-1267-3
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DOI: https://doi.org/10.1007/s00421-009-1267-3