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Assessment and comparison of in vitro immunoregulatory activity of three astaxanthin stereoisomers

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Abstract

In recent years, the immune-modulatory role of all-trans astaxanthin from different pigment sources has been studied. It was reported that all-trans astaxanthin might exist as three stereoisomers, and the composition of all-trans stereoisomers in natural materials differs from that of synthetic products. However, the different biological effects of various all-trans stereoisomers still remain unclear. In the present study, we evaluated the bioactivity of three astaxanthin stereoisomers, (3S,3’S)-trans-, (3R,3’R)-trans-and meso-trans-astaxanthin, in regulating cell-mediated immune response using mice lymphocytes and peritoneal exudates cells (PECs) systems. After the treatment with three astaxanthin stereoisomers (20 μmol L−1), the lymphocyte proliferation capacity, neutral red phagocytosis of PECs and natural killer (NK) cell cytotoxic activity were comparatively assessed. The results showed that all three astaxanthin stereoisomers significantly promoted lymphocyte proliferation, phagocytic capacity of PECs, and cytotoxic activity of NK cells. Moreover, the (3S,3’S)-trans-astaxanthin exhibited a much higher response than others.

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References

  • Amar, E. C., Kiron, V., Satoh, S., and Watanabe, T., 2001. Influence of various dietary synthetic carotenoids on bio-defense mechanisms in rainbow trout, Oncorhynchus mykiss. Aquaculture Research, 32 (Suppl 1): 162–173.

    Article  Google Scholar 

  • Amar, E. C., Kiron, V., Satoh, S., and Watanabe, T., 2004. Enhancement of innate immunity in rainbow trout (Oncorhynchus mykiss Walbaum) associated with dietary intake of carotenoids from natural products. Fish & Shellfish Immunology, 16: 527–537.

    Article  Google Scholar 

  • Amar, E. C., Kiron, V., Satoh, S., Okamoto, N., and Watanabe, T., 2002. Effects of dietary ß-carotene on the immune response of rainbow trout Oncorhynchus mykiss. Fisheries Science, 66: 1068–1075.

    Article  Google Scholar 

  • Ambati, R. R., Phang, S. M., Ravi, S., and Aswathanarayana, R. G., 2014. Astaxanthin: Sources, extraction, stability, biological activities and its commercial applications–A review. Marine Drugs, 12: 128–152.

    Article  Google Scholar 

  • Bar, E., Rise, M., Vishkautsan, M., and Arad, S., 1995. Pigment and structural changes in Chlorella zofingiensis upon light and nitrogen stress. Journal of Plant Physiology, 146: 527–534.

    Article  Google Scholar 

  • Bjerkeng, B., Peisker, M., Schwartzenberg, K., Ytrestøyl, T., and Åsgård, T., 2007. Digestibility and muscle retention of astaxanthin in Atlantic salmon, Salmo salar, fed diets with the red yeast Phaffia rhodozyma in comparison with synthetic formulated astaxanthin. Aquaculture, 269: 476–489.

    Article  Google Scholar 

  • Bjerkeng, B., Storebakken, T., and Liaaen-Jensen, S., 1992. Pigmentation of rainbow trout from start feeding to sexual maturation. Aquaculture, 108: 333–346.

    Article  Google Scholar 

  • Bon, J. A., Leathers, T. D., and Jayaswal, R. K., 1997. Isolation of astaxanthin-overproducing mutants of Phaffia rhodozyma. Biotechnology Letters, 19: 109–112.

    Article  Google Scholar 

  • Cao, Q. Z., and Lin, Z. B., 2004. Antitumor and anti-angiogenic activity of Ganoderma lucidum polysaccharides peptide. Acta Pharmacologica Sinica, 25: 833–838.

    Google Scholar 

  • Chew, B. P., Mathison, B. D., Hayek, M. G., Massimino, S., Reinhart, G. A., and Park, J. S., 2011. Dietary astaxanthin enhances immune response in dogs. Veterinary Immunology and Immunopathology, 140: 199–206.

    Article  Google Scholar 

  • Chew, B. P., Wong, M. W., Park, J. S., and Wong, T. S., 1999. Dietary beta-carotene and astaxanthin but not canthaxanthin stimulate splenocyte function in mice. Anticancer Research, 19: 5223–5227.

    Google Scholar 

  • Choubert, G., Mendes-Pinto, M. M., and Morais, R., 2006. Pigmenting efficacy of astaxanthin fed to rainbow trout Oncorhynchus mykiss: Effect of dietary astaxanthin and lipid sources. Aquaculture, 257: 429–436.

    Article  Google Scholar 

  • David, J. N., and Gordon, M. C., 2012. Natural products as sources of new drugs over the 30 years from 1981 to 2010. Journal of Natural Product, 75: 311–335.

    Article  Google Scholar 

  • Fan, L., Vonshak, A., Gabbay, R., Hirshberg, J., Cohen, Z., and Bous-siba, S., 1995. The biosynthetic pathway of astaxanthin in a green alga Haematococcus pluvialis as indicated by inhibition with diphenylamine. Plant and Cell Physiology, 36: 1519–1524.

    Google Scholar 

  • Govindaraj, J., Emmadi, P., and Puvanakrishmam, R., 2010. In vitro studies on inhibitory effect of proanthocyanidins in modulation of neutrophils and macrophages. Indian Journal of Biochemistry & Biophysics, 47: 141–147.

    Google Scholar 

  • Guerra, B. A., and Otton, R., 2011. Impact of the carotenoid astaxanthin on phagocytic capacity and ROS/RNS production of human neutrophils treated with free fatty acids and high glucose. International Immunopharmacology, 11: 2220–2226.

    Article  Google Scholar 

  • Guerra, B. A., Bolin, A. P., Morandi, A. C., and Otton R., 2012. Glycolaldehyde impairs neutrophil biochemical parameters by an oxidative and calcium-dependent mechanism-protective role of antioxidants astaxanthin and vitamin C. Diabetes Research and Clinical Practice, 98: 108–118.

    Article  Google Scholar 

  • Jurisic, V., Spuzic, I., and Konjevic, G., 1999. A comparison of the NKcell cytotoxicity with effects of TNF-a against K-562 cells, determined by LDH release assay. Cancer Letters, 138: 67–72.

    Article  Google Scholar 

  • Jyonouchi, H., Hill, R. I., Tomita, Y., and Good, R. A., 1991. Studies of immunomodulating actions of carotenoids. I. Effects of beta-carotene and astaxanthinon murine lymphocyte functions and cell surface marker expression in in vitro culture system. Nutrition and Cancer, 16: 93–105

    Google Scholar 

  • Jyonouchi, H., Zhang, L., and Tomita, Y., 1993. Studies of immunomodulating actions of carotenoids. II. Astaxanthin enhances in vitro antibody production to T-dependent antigens without facilitating polyclonal B-cell activation. Nutrition and Cancer, 19: 269–280.

    Article  Google Scholar 

  • Jyonouchi, H., Zhang, L., Gross, M., and Tomita, Y., 1994. Immunomodulating actions of carotenoids: Enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutrition and Cancer, 21: 47–58

    Article  Google Scholar 

  • Kawakami, T., Tsushima, M., Katabami, Y., Mine, M., Ishida, A., and Matsuno, T., 1998. Effect of ß, ß-carotene, ß-echinenone, astaxanthin, fucoxanthin, vitamin A and vitamin E on the biological defense of the sea urchin Pseudocentrotus depressus. Journal of Experimental Marine Biology and Ecology, 226: 165–174.

    Article  Google Scholar 

  • Konjevic, G., Juriš ic, V., and Spuzic, I., 1997. Corrections to the original lactate dehydrogenase (LDH) release assay for the evaluation of NK cell cytotoxicity. Journal of Immunological Methods, 200: 199–201.

    Article  Google Scholar 

  • Kurihara, H., Koda, H., Asami, S., Kiso, Y., and Tanaka, T., 2002. Contribution of the antioxidative property of astaxanthin to its protective effect on the promotion of cancer metastasis in mice treated with restraint stress. Life Sciences, 70: 2509–2520.

    Article  Google Scholar 

  • Macedo, R. C., Bolin, A. P., Marin, D. P., and Otton, R., 2010. Astaxanthin addition improves human neutrophils function: in vitro study. European Journal of Nutrition, 49: 447–457.

    Article  Google Scholar 

  • Moretta, A., Bottino, C., Mingari, M. C., Biassoni, R., and Moretta, L., 2002. What is a natural killer cell? Nature Immunology, 3: 6–8.

    Article  Google Scholar 

  • Moretti, V. M., Mentasti, T., Bellagamba, F., Luzzana, U., Caprino, F., Turchini, G. M., Giani, I., and Valfrè, F., 2006. Determination of astaxanthin stereoisomers and colour attributes in flesh of rainbow trout (Oncorhynchus mykiss) as a tool to distinguish the dietary pigmentation source. Food Additives and Contaminants, 23: 1056–1063.

    Article  Google Scholar 

  • Mosmann, T., 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65: 55–63.

    Article  Google Scholar 

  • Nakano, T., Kanmuri, T., Sato, M., and Takeuchi, M., 1999. Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochimica et Biophysica Acta, 1426: 119–125.

    Article  Google Scholar 

  • Otani, H., and Monnai, M., 1993. Inhibition of proliferative responses of mouse spleen lymphocytes by bovine milk casein digests. Food and Agricultural Immunology, 5: 219–229.

    Article  Google Scholar 

  • Park, J. S., Chyun, J. H., Kim, Y. K., Line, L. L., and Chew, B. P., 2010. Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutrition Metabolism and Cardiovascular Diseases, 7: 18–27.

    Google Scholar 

  • Park, J. S., Mathison, B. D., Hayek, M. G., Massimino, S., Reinhart, G. A., and Chew, B. P., 2011. Astaxanthin stimulates cell-mediated and humoral immune responses in cats. Veterinary Immunology and Immunopathology, 144: 455–461.

    Article  Google Scholar 

  • Rao, A. R., Baskaran, V., Sarada, R., and Ravishankar, G. A., 2013. In vivo bioavailability and antioxidant activity of carotenoids from micro algal biomass–A repeated dose study. Food Research International, 54: 711–717.

    Article  Google Scholar 

  • Rao, A. R., Sindhuja, H. N., Dharmesh, S. M., Sankar, K. U., Sarada, R., and Ravishankar, G. A., 2013. Effective inhibition of skin cancer, tyrosinase, and antioxidative properties by astaxanthin and astaxanthin esters from the green alga Haematococcus pluvialis. Journal of Agricultural and Food Chemistry, 61: 3842–3851.

    Article  Google Scholar 

  • Santos, S. D., Cahú, T. B., Firmino, G. O., de Castro, C. C., Carvalho, L. B. J., Bezerra, R. S., and Filho, J. L., 2012. Shrimp waste extract and astaxanthin: Rat alveolar macrophage, oxidative stress and inflammation. Journal of Food Science, 77: 141–146.

    Article  Google Scholar 

  • Schroeder, W. A., and Johnson, E. A., 1993. Antioxidant role of carotenoids in Phaffia rhodozyma. Microbiology, 139: 907–912.

    Google Scholar 

  • Storebakken, T., Foss, P., Austreng, E., and Liaaen-Jensen, S., 1985. Carotenoids in diets for salmonids: II. Epimerization studies with astaxanthin in Atlantic salmon. Aquaculture, 44: 259–269.

    Google Scholar 

  • Sun, W. H., Lin, H., Zhai, Y. X., Leng, K. L., and Xing, L. H., 2014. Separation, purification and identification of (3R,3’R)-trans-astaxanthin from Phaffia rhodozyma. Food Science, 35(11): 79–82 (in Chinese with English abstract).

    Google Scholar 

  • Takimoto, T., Takahashi, K., and Akiba, Y., 2007. Effect of dietary supplementation of astaxanthin by Phaffia rhodozyma on lipid peroxidation, drug metabolism and some immunological variables in male broiler chicks fed on diets with or without oxidised fat. British Poultry Science, 48: 90–97.

    Article  Google Scholar 

  • Thompson, I., Choubert, G., Houlihan, D. F., and Secombes, C. J., 1995. The effect of dietary vitamin A and astaxanthin on the immunocompetence of rainbow trout. Aquaculture, 133: 91–102.

    Article  Google Scholar 

  • Turujman, S. A., Wamer, W. G., Wei, R. R., and Albert, R. H., 1997. Rapid liquid chromatographic method to distinguish wild salmon from aquacultured salmon fed synthetic astaxanthin. Journal of AOAC International, 80: 622–632.

    Google Scholar 

  • Wang, C. L., Armstrong, D. W., and Chang, C. D., 2008. Rapid baseline separation of enantiomers and a mesoform of alltrans-astaxanthin, 13-cis-astaxanthin, adonirubin, and adonixanthin in standards and commercial supplements. Journal of Chromatography A, 1194: 172–177.

    Article  Google Scholar 

  • Yaqoob, P., Knapper, J. A., Webb, D. H., Williams, C. M., Newsholme, E. A., and Calder, P. C., 1998. Effect of olive oil on immune function in middle-aged men. American Journal of Clinical Nutrition, 67: 129–135.

    Google Scholar 

  • Yokota, T., Oritani, K., Takahashi, I., Ishikawa, J., Matsuyama, A., Ouchi, N., Kihara, S., Funahashi, T., Tenner, A. J., Tomiyama, Y., and Matsuzawa, Y., 2000. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood, 96: 1723–1732.

    Google Scholar 

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Sun, W., Xing, L., Lin, H. et al. Assessment and comparison of in vitro immunoregulatory activity of three astaxanthin stereoisomers. J. Ocean Univ. China 15, 283–287 (2016). https://doi.org/10.1007/s11802-016-2716-3

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  • DOI: https://doi.org/10.1007/s11802-016-2716-3

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