Skip to main content
SpringerLink
Log in

Combined fish oil and astaxanthin supplementation modulates rat lymphocyte function

European Journal of Nutrition volume 51, pages 707–718 (2012)Cite this article

Abstract

Purpose

Higher intakes of n-3 polyunsaturated fatty acids that are abundant in marine fishes have been long described as a “good nutritional intervention” with increasing clinical benefits to cardiovascular health, inflammation, mental, and neurodegenerative diseases. The present study was designed to investigate the effect of daily fish oil (FO—10 mg EPA/kg body weight (BW) and 7 mg DHA/kg BW) intake by oral gavage associated with the antioxidant astaxanthin (ASTA—1 mg/kg BW) on the redox metabolism and the functional properties of lymphocytes from rat lymph nodes.

Methods

This study was conducted by measurements of lymphocyte proliferation capacity, ROS production [superoxide (O •−2 ) and hydrogen peroxide (H2O2)], nitric oxide (NO•) generation, intracellular calcium release, oxidative damage to lipids and proteins, activities of major antioxidant enzymes, GSH/GSSG content, and cytokines release.

Results

After 45 days of FO + ASTA supplementation, the proliferation capacity of activated T- and B-lymphocytes was significantly diminished followed by lower levels of O •−2 , H2O2 and NO• production, and increased activities of total/SOD, GR and GPx, and calcium release in cytosol. ASTA was able to prevent oxidative modification in cell structures through the suppression of the oxidative stress condition imposed by FO. l-selectin was increased by FO, and IL-1β was decreased only by ASTA supplementation.

Conclusion

We can propose that association of ASTA with FO could be a good strategy to prevent oxidative stress induced by polyunsaturated fatty acids and also to potentiate immuno-modulatory effects of FO.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Calder PC (2009) Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie. doi:10.1016/j.biochi.2009.01.008

  2. Calder PC, Yaqoob P (2009) Understanding omega-3 polyunsaturated fatty acids. Postgrad Med 121:148–157. doi:10.3810/pgm.2009.11.2083

    Article  Google Scholar 

  3. Fortin PR, Lew RA, Liang MH, Wright EA, Beckett LA, Chalmers TC, Sperling RI (1995) Validation of a meta-analysis: the effects of fish oil in rheumatoid arthritis. J Clin Epidemiol 48:1379–1390

    Article  CAS  Google Scholar 

  4. De Caterina R, Cybulsky MI, Clinton SK, Gimbrone MA Jr, Libby P (1994) The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arterioscler Thromb 14:1829–1836

    Article  Google Scholar 

  5. Hughes DA, Southon S, Pinder AC (1996) (n-3) Polyunsaturated fatty acids modulate the expression of functionally associated molecules on human monocytes in vitro. J Nutr 126:603–610

    CAS  Google Scholar 

  6. De Caterina R, Libby P (1996) Control of endothelial leukocyte adhesion molecules by fatty acids. Lipids 31(Suppl):S57–S63

    Article  Google Scholar 

  7. Hughes DA, Pinder AC, Piper Z, Johnson IT, Lund EK (1996) Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes. Am J Clin Nutr 63:267–272

    CAS  Google Scholar 

  8. Calder PC (2006) Polyunsaturated fatty acids and inflammation. Prostaglandins Leukot Essent Fatty Acids 75:197–202. doi:10.1016/j.plefa.2006.05.012

    Article  CAS  Google Scholar 

  9. Collie-Duguid ES, Wahle KW (1996) Inhibitory effect of fish oil n-3 polyunsaturated fatty acids on the expression of endothelial cell adhesion molecules. Biochem Biophys Res Commun 220:969–974. doi:10.1006/bbrc.1996.0516

    Article  CAS  Google Scholar 

  10. Sanderson P, Calder PC (1998) Dietary fish oil diminishes lymphocyte adhesion to macrophage and endothelial cell monolayers. Immunology 94:79–87

    Article  CAS  Google Scholar 

  11. Calder PC, Yaqoob P, Thies F, Wallace FA, Miles EA (2002) Fatty acids and lymphocyte functions. Br J Nutr 87(Suppl 1):S31–S48

    Article  CAS  Google Scholar 

  12. Deckelbaum RJ, Calder PC (2010) Dietary n-3 and n-6 fatty acids: are there ‘bad’ polyunsaturated fatty acids? Curr Opin Clin Nutr Metab Care 13:123–124. doi:10.1097/MCO.0b013e328336696d

    Google Scholar 

  13. Barros MP, Pinto E, Colepicolo P, Pedersen M (2001) Astaxanthin and peridinin inhibit oxidative damage in Fe(2+)-loaded liposomes: scavenging oxyradicals or changing membrane permeability? Biochem Biophys Res Commun 288:225–232. doi:10.1006/bbrc.2001.5765

    Article  CAS  Google Scholar 

  14. Palozza P, Krinsky NI (1992) Astaxanthin and canthaxanthin are potent antioxidants in a membrane model. Arch Biochem Biophys 297:291–295

    Article  CAS  Google Scholar 

  15. Iwamoto T, Hosoda K, Hirano R, Kurata H, Matsumoto A, Miki W, Kamiyama M, Itakura H, Yamamoto S, Kondo K (2000) Inhibition of low-density lipoprotein oxidation by astaxanthin. J Atheroscler Thromb 7:216–222

    CAS  Google Scholar 

  16. Iwamoto T, Hosoda K, Hirano R, Kurata H, Matsumoto A, Miki W, Kamiyama M, Itakura H, Yamamoto S, Kondo K (2000) Inhibition of low-density lipoprotein oxidation by astaxanthin. J Atheroscler Thromb 7:216–222

    CAS  Google Scholar 

  17. Jacobsson LS, Yuan XM, Zieden B, Olsson AG (2004) Effects of alpha-tocopherol and astaxanthin on LDL oxidation and atherosclerosis in WHHL rabbits. Atherosclerosis 173:231–237. doi:10.1016/j.atherosclerosis.2004.01.003

    CAS  Google Scholar 

  18. Ohgami K, Shiratori K, Kotake S, Nishida T, Mizuki N, Yazawa K, Ohno S (2003) Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Invest Ophthalmol Vis Sci 44:2694–2701

    Article  Google Scholar 

  19. Naito Y, Uchiyama K, Aoi W, Hasegawa G, Nakamura N, Yoshida N, Maoka T, Takahashi J, Yoshikawa T (2004) Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors 20:49–59

    Article  CAS  Google Scholar 

  20. Hussein G, Sankawa U, Goto H, Matsumoto K, Watanabe H (2006) Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod 69:443–449. doi:10.1021/np050354+

    Article  CAS  Google Scholar 

  21. Conroy DM, Stubbs CD, Belin J, Pryor CL, Smith AD (1986) The effects of dietary (n-3) fatty acid supplementation on lipid dynamics and composition in rat lymphocytes and liver microsomes. Biochim Biophys Acta 861:457–462

    Article  CAS  Google Scholar 

  22. Otton R, Carvalho CR, Mendonca JR, Curi R (2002) Low proliferation capacity of lymphocytes from alloxan-diabetic rats: involvement of high glucose and tyrosine phosphorylation of Shc and IRS-1. Life Sci 71:2759–2771

    Article  CAS  Google Scholar 

  23. Pick E, Mizel D (1981) Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. J Immunol Methods 46:211–226

    Article  CAS  Google Scholar 

  24. Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141:2407–2412

    CAS  Google Scholar 

  25. Otton R, da Silva DO, Campoio TR, Silveira LR, de Souza MO, Hatanaka E, Curi R (2007) Non-esterified fatty acids and human lymphocyte death: a mechanism that involves calcium release and oxidative stress. J Endocrinol 195:133–143. doi:10.1677/JOE-07-0195

    Article  CAS  Google Scholar 

  26. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

    CAS  Google Scholar 

  27. Otton R, Graziola F, Hirata MH, Curi R, Williams JF (1998) Dietary fats alter the activity and expression of glucose-6-phosphate dehydrogenase in rat lymphoid cells and tissues. Biochem Mol Biol Int 46:529–536

    CAS  Google Scholar 

  28. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  29. Mannervik B (1985) Glutathione peroxidase. Methods Enzymol 113:490–495

    Article  CAS  Google Scholar 

  30. Ewing JF, Janero DR (1995) Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232:243–248

    Article  CAS  Google Scholar 

  31. Fraga CG, Leibovitz BE, Tappel AL (1988) Lipid peroxidation measured as thiobarbituric acid-reactive substances in tissue slices: characterization and comparison with homogenates and microsomes. Free Radic Biol Med 4:155–161

    Article  CAS  Google Scholar 

  32. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984. doi:10.1038/nature02075

    Article  CAS  Google Scholar 

  33. Murphy ME, Kehrer JP (1989) Oxidation state of tissue thiol groups and content of protein carbonyl groups in chickens with inherited muscular dystrophy. Biochem J 260:359–364

    CAS  Google Scholar 

  34. Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165. doi:10.1038/nprot.2006.378

    Article  CAS  Google Scholar 

  35. 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 72:248–254

    Article  CAS  Google Scholar 

  36. Calder PC (2007) Immunological parameters: what do they mean? J Nutr 137:773S–780S

    CAS  Google Scholar 

  37. Bolin AP, Macedo RC, Marin DP, Barros MP, Otton R (2010) Astaxanthin prevents in vitro auto-oxidative injury in human lymphocytes. Cell Biol Toxicol 26:457–467. doi:10.1007/s10565-010-9156-4

    Google Scholar 

  38. Pompeia C, Lopes LR, Miyasaka CK, Procopio J, Sannomiya P, Curi R (2000) Effect of fatty acids on leukocyte function. Braz J Med Biol Res 33:1255–1268

    Article  CAS  Google Scholar 

  39. Wang H, Xie X, Lu WG, Ye DF, Chen HZ, Li X, Cheng Q (2004) Ovarian carcinoma cells inhibit T cell proliferation: suppression of IL-2 receptor beta and gamma expression and their JAK-STAT signaling pathway. Life Sci 74:1739–1749

    Article  CAS  Google Scholar 

  40. Gorjao R, Cury-Boaventura MF, de Lima TM, Curi R (2007) Regulation of human lymphocyte proliferation by fatty acids. Cell Biochem Funct 25:305–315. doi:10.1002/cbf.1388

    Article  CAS  Google Scholar 

  41. Denys A, Hichami A, Khan NA (2005) n-3 PUFAs modulate T-cell activation via protein kinase C-alpha and -epsilon and the NF-kappa B signaling pathway. J Lipid Res 46:752–758. doi:10.1194/jlr.M400444-JLR200

    Article  CAS  Google Scholar 

  42. Bhuvaneswari V, Nagini S (2005) Lycopene: a review of its potential as an anticancer agent. Curr Med Chem Anticancer Agents 5:627–635

    Article  CAS  Google Scholar 

  43. Huang CS, Shih MK, Chuang CH, Hu ML (2005) Lycopene inhibits cell migration and invasion and upregulates Nm23–H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells. J Nutr 135:2119–2123

    CAS  Google Scholar 

  44. Kim YH, Koh HK, Kim DS (2010) Down-regulation of IL-6 production by astaxanthin via ERK-, MSK-, and NF-kappa B-mediated signals in activated microglia. Int Immunopharmacol 10:1560–1572. doi:10.1016/j.intimp.2010.09.007

  45. Odeberg JM, Kaufmann P, Kroon KG, Hoglund P (2003) Lipid drug delivery and rational formulation design for lipophilic drugs with low oral bioavailability, applied to cyclosporine. Eur J Pharm Sci 20:375–382

    Article  CAS  Google Scholar 

  46. Okada Y, Ishikura M, Maoka T (2009) Bioavailability of astaxanthin in Haematococcus algal extract: the effects of timing of diet and smoking habits. Biosci Biotechnol Biochem 73:1928–1932

    Article  CAS  Google Scholar 

  47. Petri D, Lundebye AK (2007) Tissue distribution of astaxanthin in rats following exposure to graded levels in the feed. Comp Biochem Physiol C Toxicol Pharmacol 145:202–209. doi:10.1016/j.cbpc.2006.12.008

    Article  Google Scholar 

  48. Razzaq TM, Ozegbe P, Jury EC, Sembi P, Blackwell NM, Kabouridis PS (2004) Regulation of T-cell receptor signalling by membrane microdomains. Immunology 113:413–426. doi:10.1111/j.1365-2567.2004.01998.x

    Article  CAS  Google Scholar 

  49. Harder T (2004) Lipid raft domains and protein networks in T-cell receptor signal transduction. Curr Opin Immunol 16:353–359. doi:10.1016/j.coi.2004.03.013

    Article  CAS  Google Scholar 

  50. Wu M, Harvey KA, Ruzmetov N, Welch ZR, Sech L, Jackson K, Stillwell W, Zaloga GP, Siddiqui RA (2005) Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int J Cancer 117:340–348. doi:10.1002/ijc.21238

    Article  CAS  Google Scholar 

  51. Meydani M, Azzi A (2009) Diabetes risk: antioxidants or lifestyle? Am J Clin Nutr 90:253–254. doi:10.3945/ajcn.2009.28177

    Article  CAS  Google Scholar 

  52. Roth S, Droge W (1987) Regulation of T-cell activation and T-cell growth factor (TCGF) production by hydrogen peroxide. Cell Immunol 108:417–424

    Article  CAS  Google Scholar 

  53. Keyse SM, Tyrrell RM (1990) Induction of the heme oxygenase gene in human skin fibroblasts by hydrogen peroxide and UVA (365 nm) radiation: evidence for the involvement of the hydroxyl radical. Carcinogenesis 11:787–791

    Article  CAS  Google Scholar 

  54. Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10:2247–2258

    CAS  Google Scholar 

  55. Luostarinen R, Saldeen T (1996) Dietary fish oil decreases superoxide generation by human neutrophils: relation to cyclooxygenase pathway and lysosomal enzyme release. Prostaglandins Leukot Essent Fatty Acids 55:167–172

    Article  CAS  Google Scholar 

  56. Fisher M, Levine PH, Weiner BH, Johnson MH, Doyle EM, Ellis PA, Hoogasian JJ (1990) Dietary n-3 fatty acid supplementation reduces superoxide production and chemiluminescence in a monocyte-enriched preparation of leukocytes. Am J Clin Nutr 51:804–808

    CAS  Google Scholar 

  57. Tayyebi-Khosroshahi H, Houshyar J, Tabrizi A, Vatankhah AM, Razzagi Zonouz N, Dehghan-Hesari R (2010) Effect of omega-3 fatty acid on oxidative stress in patients on hemodialysis. Iran J Kidney Dis 4(4):322–326

    Google Scholar 

  58. Kim SJ, Zhang Z, Saha A, Sarkar C, Zhao Z, Xu Y, Mukherjee AB (2010) Omega-3 and omega-6 fatty acids suppress ER- and oxidative stress in cultured neurons and neuronal progenitor cells from mice lacking PPT1. Neurosci Lett 479:292–296. doi:10.1016/j.neulet.2010.05.083

    Google Scholar 

  59. Komatsu W, Ishihara K, Murata M, Saito H, Shinohara K (2003) Docosahexaenoic acid suppresses nitric oxide production and inducible nitric oxide synthase expression in interferon-gamma plus lipopolysaccharide-stimulated murine macrophages by inhibiting the oxidative stress. Free Radic Biol Med 34:1006–1016

    Article  CAS  Google Scholar 

  60. Lu G, Greene EL, Nagai T, Egan BM (1998) Reactive oxygen species are critical in the oleic acid-mediated mitogenic signaling pathway in vascular smooth muscle cells. Hypertension 32:1003–1010

    Article  CAS  Google Scholar 

  61. Kelley DS, Hubbard NE, Erickson KL (2005) Regulation of human immune and inflammatory responses by dietary fatty acids. Adv Food Nutr Res 50:101–138. doi:10.1016/S1043-4526(05)50004-4

    Article  CAS  Google Scholar 

  62. Fritsche K (2006) Fatty acids as modulators of the immune response. Annu Rev Nutr 26:45–73. doi:10.1146/annurev.nutr.25.050304.092610

    Article  CAS  Google Scholar 

  63. Lecchi C, Invernizzi G, Agazzi A, Ferroni M, Pisani LF, Savoini G, Ceciliani F (2011) In vitro modulation of caprine monocyte immune functions by omega-3 polyunsaturated fatty acids. Vet J 189(3):353–355. doi:10.1016/j.tvjl.2010.09.001

    Google Scholar 

  64. Guimaraes AR, Curi R (1991) Metabolic changes induced by w-3 polyunsaturated fatty acid rich-diet (w-3 PUFA) on the thymus, spleen and mesenteric lymph nodes of adult rats. Biochem Int 25:689–695

    CAS  Google Scholar 

  65. Krinsky NI, Johnson EJ (2005) Carotenoid actions and their relation to health and disease. Mol Aspects Med 26:459–516. doi:10.1016/j.mam.2005.10.001

    Article  CAS  Google Scholar 

  66. Nakano M, Onodera A, Saito E, Tanabe M, Yajima K, Takahashi J, Nguyen VC (2008) Effect of astaxanthin in combination with alpha-tocopherol or ascorbic acid against oxidative damage in diabetic ODS rats. J Nutr Sci Vitaminol 54:329–334

    Article  CAS  Google Scholar 

  67. Ikeuchi M, Koyama T, Takahashi J, Yazawa K (2007) Effects of astaxanthin in obese mice fed a high-fat diet. Biosci Biotechnol Biochem 71:893–899

    Article  CAS  Google Scholar 

  68. Naguib YM (2000) Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 48:1150–1154

    Article  CAS  Google Scholar 

  69. Brechard S, Tschirhart EJ (2008) Regulation of superoxide production in neutrophils: role of calcium influx. J Leukoc Biol 84:1223–1237. doi:10.1189/jlb.0807553

    Article  CAS  Google Scholar 

  70. Prasad A, Bloom MS, Carpenter DO (2010) Role of calcium and ROS in cell death induced by polyunsaturated fatty acids in murine thymocytes. J Cell Physiol 225:829–836. doi:10.1002/jcp.22290

    Google Scholar 

  71. Yog R, Barhoumi R, McMurray DN, Chapkin RS (2010) n-3 polyunsaturated fatty acids suppress mitochondrial translocation to the immunologic synapse and modulate calcium signaling in T cells. J Immunol 184(10):5865–5873. doi:10.4049/jimmunol.0904102

    Google Scholar 

  72. Lin TY, Lu CW, Wang SJ (2010) Astaxanthin inhibits glutamate release in rat cerebral cortex nerve terminals via suppression of voltage-dependent Ca(2+) entry and mitogen-activated protein kinase signaling pathway. J Agric Food Chem 58:8271–8278. doi:10.1021/jf101689t

    Google Scholar 

  73. Macedo RC, Bolin AP, Marin DP, Otton R (2010) Astaxanthin addition improves human neutrophils function: in vitro study. Eur J Nutr 49:447–457. doi:10.1007/s00394-010-0103-1

    Google Scholar 

  74. Maoka T, Etoh T, Kishimoto S, Sakata S (2011) Carotenoids and their fatty acid esters in the petals of Adonis aestivalis. J Oleo Sci 60:47–52

    Google Scholar 

  75. Wu TH, Liao JH, Hou WC, Huang FY, Maher TJ, Hu CC (2006) Astaxanthin protects against oxidative stress and calcium-induced porcine lens protein degradation. J Agric Food Chem 54:2418–2423. doi:10.1021/jf052651q76

    Article  CAS  Google Scholar 

  76. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G (2005) Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11:90–94. doi:10.1038/nm1168

    Article  CAS  Google Scholar 

  77. Picker LJ, Butcher EC (1992) Physiological and molecular mechanisms of lymphocyte homing. Annu Rev Immunol 10:561–591. doi:10.1146/annurev.iy.10.040192.003021

    Article  CAS  Google Scholar 

  78. Mora C, Grewal IS, Wong FS, Flavell RA (2004) Role of l-selectin in the development of autoimmune diabetes in non-obese diabetic mice. Int Immunol 16:257–264

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are indebted to the constant assistance of Geraldo, TP. This research is supported by Fundação de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP 07/03334-6, 2009/12342-8, and 2002/09405-9), Universidade Cruzeiro do Sul, and Departamento de Psicobiologia—UNIFESP/Associação Fundo de Incentivo à Psicofarmacologia (AFIP). Dr. Marcelo Paes de Barros is also indebted to the International Foundation for Science (F/3816-1) for additional funds and to Dr. Åke Lignell from BioReal AB/Fuji Chemicals (Sweden/Japan) for supplying astaxanthin-rich algal biomass for in vivo studies.

Conflict of interest

The authors declare they have no competing financial interests.

Author information

Authors and Affiliations

  1. Postgraduate Program, Health Sciences, CBS, Cruzeiro do Sul University, Av. Regente Feijó, 1295, Sao Paulo, SP, 03342000, Brazil

    Rosemari Otton, Douglas Popp Marin, Anaysa Paola Bolin, Rita de Cássia Santos Macedo, Thais Regina Campoio, Claudio Fineto Jr., Beatriz Alves Guerra & Marcelo Paes Barros

  2. Postgraduate Program, Human Movement Sciences Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, Sao Paulo, SP, 01506000, Brazil

    Marcelo Paes Barros

  3. Departamento de Psicobiologia, Universidade Federal de São Paulo UNIFESP, São Paulo, 04023062, Brazil

    José Roberto Leite & Rita Mattei

Authors
  1. Rosemari Otton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas Popp Marin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anaysa Paola Bolin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rita de Cássia Santos Macedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thais Regina Campoio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Claudio Fineto Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Beatriz Alves Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. José Roberto Leite
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marcelo Paes Barros
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Rita Mattei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosemari Otton.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Otton, R., Marin, D.P., Bolin, A.P. et al. Combined fish oil and astaxanthin supplementation modulates rat lymphocyte function. Eur J Nutr 51, 707–718 (2012). https://doi.org/10.1007/s00394-011-0250-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-011-0250-z

Keywords

search

Navigation