Marine carotenoids: Bioactivities and potential benefits to human health

Critical Reviews in Food Science and Nutrition

Volumn 57, Issue 12, 2017, Pages 2600-2610

  Chuyen, Hoang Van ^a,b   Eun, Jong Bang ^a  

^a Chonnam National University   (South Korea)

^b TAY NGUYEN UNIVERSITY   (Viet Nam)

Author keywords

astaxanthin; Biological activity; cantaxanthin; fucoxanthin

Indexed keywords

ANIMALS; BIOACTIVITY; MARINE BIOLOGY; PHYSIOLOGY;

ANTI-INFLAMMATORIES; ASTAXANTHIN; CANTAXANTHIN; FUCOXANTHIN; MARINE ORGANISMS; NATURAL PIGMENT; PHYSIOLOGICAL FUNCTIONS; POTENTIAL BENEFITS;

PIGMENTS;

ANTIDIABETIC AGENT; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; BIOLOGICAL PRODUCT; CAROTENOID; XANTHOPHYLL;

ANIMAL; AQUATIC SPECIES; CHEMISTRY; HUMAN; PHYSIOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; AQUATIC ORGANISMS; BIOLOGICAL PRODUCTS; CAROTENOIDS; HUMANS; HYPOGLYCEMIC AGENTS; XANTHOPHYLLS;

EID: 85018407954     PISSN: 10408398     EISSN: 15497852     Source Type: Journal    
DOI: 10.1080/10408398.2015.1063477     Document Type: Review

References (77)

1. Abdel-Fatth, G., Watzl, B., Huang, D., and Watson, R. R., (1993). Beta-carotene in vitro stimulates tumor necrosis factor alpha and interleukin 1 alpha secretion by human peripheral blood mononuclear cells. Nutr. Res. 13:863–871.
2. Abidov, M., Ramazanov, Z., Seifulla, R., and Grachev, S., (2010). The effects of Xanthigen in the weight management of obese premenopausal women with non-alcoholic fatty liver disease and normal liver fat. Diabetes Obes. Metab. 12:72–81.
3. Arunkumar, E., Bhuvaneswari, S., and Anuradha, C. V., (2012). An intervention study in obese mice with astaxanthin, a marine carotenoid–effects on insulin signaling and pro-inflammatory cytokines. Food Funct. 3:120–126.
4. Asai, A., Sugawara, T., Ono, H., and Nagao, A., (2004). Biotransformation of fucoxanthinol into amarouciaxanthin A in mice and HepG2 cells:formation and cytotoxicity of fucoxanthin metabolites. Drug Metab Dispos. 32:205–211.
5. Asai, A., Yonekura, L., and Nagao, A., (2008). Low bioavailability of dietary epoxyxanthophylls in humans. Br J Nutr. 100:273–277.
6. Bennedsen, M., Wang, X., Willen, R., Wadstrom, T., and Andersen, L. P., (1999). Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol. Lett. 70:185–189.
7. Berge, R. K., Madsen, L., Vaagenes, H., Tronstad, K. J., Gottlicher, M., and Rustan, A. C., (1999). In contrast with docosahexaenoic acid, eicosapentaenoic acid and hypolipidaemic derivatives decrease hepatic synthesis and secretion of triacylglycerol by decreased diacylglycerol acyltransferase activity and stimulation of fatty acid oxidation. Biochem. J. 343:191–197.
8. Bhuvaneswari, S., and Anuradha, C. V., (2012). Astaxanthin prevents loss of insulin signaling and improves glucose metabolism in liver of insulin resistant mice. Canadian J. Physiol. Pharmacol. 90:1544–1552.
9. Bhuvaneswari, S., Arunkumar, E., Viswanathan, P., and Anuradha, C. V., (2010). Astaxanthin restricts weight gain, promotes insulin sensitivity and curtails fatty liver disease in mice fed a obesity-promoting diet. Process Biochem. 45:1406–1414.
10. Chew, B. P., Park, J. S., Wong, M. W., and Wong, T. S., (1999). A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res. 19:1849–1853.
11. Choi, S. K., Park, Y. S., Choi, D. K., and Chang, H. I., (2008). Effects of astaxanthin on the production of NO and the expression of COX-2 and iNOS in LPS-stimulated BV2 microglial cells. J Microbiol. Biotechnol. 18:1996.
12. Clark, R. M., and Furr, H. C., (2001). Absorption of canthaxanthin by the rat is influenced by total lipid in the intestinal lumen. Lipids. 36:473–475.
13. Clark, R. M., Yao, L., She, L., and Furr, H. C., (1998). A comparison of lycopene and canthaxanthin absorption:Using the rat to study the absorption of non-provitamin A carotenoids. Lipids. 33:159–163.
14. Clark, R. M., Yao, L., She, L., and Furr, H. C., (2000). A comparison of lycopene and astaxanthin absorption from corn oil and olive oil emulsions. Lipids. 35:803–806.
15. Ghidalia, W., (1985). The Biology of Crustacea. Academic Press, New York.
16. Gronn, M., Christensen, E., Hagve, T. A., and Christophersen, B. O., (1992). Effects of dietary purified eicosapentaenoic acid (20:5 (n-3)) and docosahexaenoic acid (22:6(n-3)) on fatty acid desaturation and oxidation in isolated rat liver cells. Biochim. Biophys. Acta. 1125:35–43.
17. Gross, J., (1991). Pigments in Vegetables:Chlorophylls and Carotenoids. Van Nostrand Reinhold, New York.
18. Grubbs, C. J., Eto, I., Juliana, M. M., and Whitaker, L. M., (1991). Effect of canthaxanthin on chemically induced mammary carcinogenesis. Oncology. 48:239–245.
19. Hanusch, M., Stahl, W., Schulz, W. A., and Sies, H., (1995). Induction of gap junctional communication by 4-oxoretinoic acid generated from its precursor canthaxanthin. Arch. Biochem. Biophys. 317:423–428.
20. Hosokawa, M., Kudo, M., Maeda, H., Kohno, H., Tanaka, T., and Miyashita, K., (2004). Fucoxanthin induces apoptosis and enhances the antiproliferative effect of the PPARgamma ligand, troglitazone, on colon cancer cells. Biochim. Biophys. Acta. 1675:113–119.
21. Hosokawa, M., Okada, T., Mikami, N., Konishi, I., and Miyashita, K., (2009). Bio-functions of marine carotenoids. Food Sci. Biotechnol. 18:1–11.
22. Hosokawa, M., Wanezaki, S., Miyauchi, K., Kurihara, H., Kohno, H., Kawabata, J., Takahashi, K. (1999). Apoptosis-inducing effect of fucoxanthin on human leukemia cell HL-60. Food Sci. Technol. Res. 5:243–246.
23. Huang, D. S., Odeleye, O. E., and Watson, R. R., (1992). Inhibitory effects of canthaxanthin on in vitro growth of murine tumor cells. Cancer Lett. 65:209–213.
24. Hussein, G., Goto, H., Oda, S., Sankawa, U., Matsumoto, K., and Watanabe, H., (2006). Antihypertensive potential and mechanism of action of astaxanthin:III. Antioxidant and histopathological effects in spontaneously hypertensive rats. Biol. Pharm. Bull. 29:684–688.
25. Hussein, G., Nakagawa, T., Goto, H., Shimada, Y., Matsumoto, K., Sankawa, U., and Watanabe, H., (2007). Astaxanthin ameliorates features of metabolic syndrome in SHR/NDmcr-cp. Life Sci. 80:522–529.
26. Hussein, G., Nakamura, M., Zhao, Q., Iguchi, T., Goto, H., Sankawa, U., and Watanabe, H., (2005). Antihypertensive and neuroprotective effects of astaxanthin in experimental animals. Biol. Pharm. Bull. 28:47–52.
27. Ikeuchi, M., Koyama, T., Takahashi, J., and Yazawa, K., (2007). Effects of astaxanthin in obese mice fed a high-fat diet. Biosci. Biotechnol. Biochem. 71:893–899.
28. Iwamoto, T., Hosoda, K., Hirano, R., Kurata, H., Matsumoto, A., Miki, W., Kondo, K., (2000). Inhibition of low-density lipoprotein oxidation by astaxanthin. J Atheroscler Thromb. 7:216–222.
29. Jyonouchi, H., Sun, S., Iijima, K., and Gross, M. D., (2000). Antitumor activity of astaxanthin and its mode of action. Nutr Cancer. 36:59–65.
30. Katsumura, N., Okuno, M., Onogi, N., Moriwaki, H., Muto, Y., and Kojima, S., (1996). Suppression of mouse skin papilloma by canthaxanthin and beta-carotene in vivo:Possibility of the regression of tumorigenesis by carotenoids without conversion to retinoic acid. Nutr. Cancer. 26:203–208.
31. Kim, J. M., Araki, S., Kim, D. J., Park, C. B., Takasuka, N., Baba-Toriyama, H., Tsuda, H., (1998). Chemopreventive effects of carotenoids and curcumins on mouse colon carcinogenesis after 1,2-dimethylhydrazine initiation. Carcinogenesis. 19:81–85.
32. Kim, K. N., Heo, S. J., Kang, S. M., Ahn, G., and Jeon, Y. J., (2010). Fucoxanthin induces apoptosis in human leukemia HL-60 cells through a ROS-mediated Bcl-xL pathway. Toxicol In Vitro. 24:1648–1654.
33. Konishi, I., Hosokawa, M., Sashima, T., Kobayashi, H., and Miyashita, K., (2006). Halocynthiaxanthin and fucoxanthinol isolated from Halocynthia roretzi induce apoptosis in human leukemia, breast and colon cancer cells. Compar. Biochem.Physiol. Part C:Toxicol. Pharmacol. 142:53–59.
34. Kotake-Nara, E., Asai, A., and Nagao, A., (2005). Neoxanthin and fucoxanthin induce apoptosis in PC-3 human prostate cancer cells. Cancer Lett. 220:75–84.
35. Kotake-Nara, E., Kushiro, M., Zhang, H., Sugawara, T., Miyashita, K., and Nagao, A., (2001). Carotenoids affect proliferation of human prostate cancer cells. J. Nutr. 131:3303–3306.
36. Kotake-Nara, E., Sugawara, T., and Nagao, A., (2005). Antiproliferative effect of neoxanthin and fucoxanthin on cultured cells. Fisheries Sci. 71:459–461.
37. Kozuki, Y., Miura, Y., and Yagasaki, K., (2000). Inhibitory effects of carotenoids on the invasion of rat ascites hepatoma cells in culture. Cancer Lett. 151:111–115.
38. Krinsky, N. I., and Johnson, E. J., (2005). Carotenoid actions and their relation to health and disease. Mol. Aspects. Med. 26:459–516.
39. 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 Sci. 70:2509–2520.
40. Lee, S. J., Bai, S. K., Lee, K. S., Namkoong, S., Na, H. J., Ha, K. S., Kim, Y. M., (2003). Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing I(kappa)B kinase-dependent NF-kappaB activation. Mol. Cells. 16:97–105.
41. Leite, M. F., Lima, A. M., Massuyama, M. M., and Otton, R., (2010). Astaxanthin restores the enzymatic antioxidant profile in salivary gland of alloxan-induced diabetic rats. Arch. Oral Biol. 55:479–485.
42. Lyons, N. M., and O'Brien, N. M., (2002). Modulatory effects of an algal extract containing astaxanthin on UVA-irradiated cells in culture. J. Dermatol. Sci. 30:73–84.
43. Macedo, R. C., Bolin, A. P., Marin, D. P., and Otton, R., (2010). Astaxanthin addition improves human neutrophils function:in vitro study. Eur J. Nutr. 49:447–457.
44. Maeda, H., Hosokawa, M., Sashima, T., Funayama, K., and Miyashita, K., (2005). Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem. Biophys. Res. Commun. 332:392–397.
45. Maeda, H., Hosokawa, M., Sashima, T., and Miyashita, K., (2007). Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-Ay mice. J. Agric. Food Chem. 55:7701–7706.
46. Maeda, H., Hosokawa, M., Sashima, T., Takahashi, N., Kawada, T., and Miyashita, K., (2006). Fucoxanthin and its metabolite, fucoxanthinol, suppress adipocyte differentiation in 3T3-L1 cells. Int. J. Mol. Med. 18:147–152.
47. Matsumoto, M., Hosokawa, M., Matsukawa, N., Hagio, M., Shinoki, A., Nishimukai, M., Hara, H., (2010). Suppressive effects of the marine carotenoids, fucoxanthin and fucoxanthinol on triglyceride absorption in lymph duct-cannulated rats. Eur. J. Nutr. 49:243–249.
48. Matsuno, T., (2001). Aquatic animal carotenoids. Fisheries Sci. 67:771–783.
49. Mein, J. R., Lian, F., and Wang, X. D., (2008). Biological activity of lycopene metabolites:Implications for cancer prevention. Nutr. Rev. 66:667–683.
50. Mercke, O. J., Lignell, A., Pettersson, A., and Hoglund, P., (2003). Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur. J. Pharm Sci. 19:299–304.
51. Miyawaki, H., Takahashi, J., Tsukahara, H., and Takehara, I., (2008). Effects of astaxanthin on human blood rheology. J. Clin. Biochem Nutr. 43:69–74.
52. Molnar, P., Kawase, M., Satoh, K., Sohara, Y., Tanaka, T., Tani, S., Molnar, J. (2005). Biological activity of carotenoids in red paprika, Valencia orange and Golden delicious apple. Phytother. Res. 19:700–707.
53. Muto, Y., Fujii, J., Shidoji, Y., Moriwaki, H., Kawaguchi, T., and Noda, T., (1995). Growth retardation in human cervical dysplasia-derived cell lines by beta-carotene through down-regulation of epidermal growth factor receptor. Am. J. Clin. Nutr. 62:1535S–1540S.
54. Nakao, R., Nelson, O. L., Park, J. S., Mathison, B. D., Thompson, P. A., and Chew, B. P., (2010). Effect of astaxanthin supplementation on inflammation and cardiac function in BALB/c mice. Anticancer Res. 30:2721–2725.
55. Nishino, H., Tsushima, M., Matsuno, T., Tanaka, Y., Okuzumi, J., Murakoshi, M., et al. (1992). Anti-neoplastic effect of halocynthiaxanthin, a metabolite of fucoxanthin. Anticancer Drugs. 3:493–497.
56. Nogueira, F. N., Carvalho, A. M., Yamaguti, P. M., and Nicolau, J., (2005). Antioxidant parameters and lipid peroxidation in salivary glands of streptozotocin-induced diabetic rats. Clin. Chim. Acta. 353:133–139.
57. Ohgami, K., Shiratori, K., Kotake, S., Nishida, T., Mizuki, N., Yazawa, K., and Ohno, S., (2003). Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Invest. Ophthalmol. Vis. Sci. 44:2694–2701.
58. Okada, T., Mizuno, Y., Sibayama, S., Hosokawa, M., and Miyashita, K., (2011). Antiobesity effects of Undaria lipid capsules prepared with scallop phospholipids. J. Food Sci. 76:H2–6.
59. Palan, P. R., Mikhail, M. S., Goldberg, G. L., Basu, J., Runowicz, C. D., and Romney, S. L., (1996). Plasma levels of beta-carotene, lycopene, canthaxanthin, retinol, and alpha- and tau-tocopherol in cervical intraepithelial neoplasia and cancer. Clin. Cancer Res. 2:181–185.
60. Palozza, P., Calviello, G., Serini, S., Moscato, P., Luberto, C., and Bartoli, G. M., (1997). Antitumor effect of an oral administration of canthaxanthin on BALB/c mice bearing thymoma cells. Nutr. Cancer. 28:199–205.
61. Palozza, P., Maggiano, N., Calviello, G., Lanza, P., Piccioni, E., Ranelletti, F. O., and Bartoli, G. M., (1998). Canthaxanthin induces apoptosis in human cancer cell lines. Carcinogenesis. 19:373–376.
62. 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. Nutr. Metab. (Lond). 7:18.
63. Preuss, H. G., Echard, B., Yamashita, E., and Perricone, N. V., (2011). High dose astaxanthin lowers blood pressure and increases insulin sensitivity in rats:are these effects interdependent? Int. J. Med. Sci. 8:126–138.
64. Sangeetha, R. K., Bhaskar, N., Divakar, S., and Baskaran, V., (2010). Bioavailability and metabolism of fucoxanthin in rats:structural characterization of metabolites by LC-MS (APCI). Mol. Cell. Biochem. 333:299–310.
65. Sharoni, Y., Agemy, L., Giat, U., Kirilov, E., Danilenko, M., and Levy, J., (2002). Lycopene and astaxanthin inhibit human prostate cancer cell proliferation induced by androgens. Paper presented at the 13th Int. Carotenoid Symp, Honolulu, 6–11 January 2002.
66. Shiratori, K., Ohgami, K., Ilieva, I., Jin, X. H., Koyama, Y., Miyashita, K., Ohno, S., (2005). Effects of fucoxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Exp. Eye Res. 81:422–428.
67. Speranza, L., Pesce, M., Patruno, A., Franceschelli, S., de Lutiis, M. A., Grilli, A., and Felaco, M., (2012). Astaxanthin treatment reduced oxidative induced pro-inflammatory cytokines secretion in U937:SHP-1 as a novel biological target. Mar. Drugs. 10:890–899.
68. Sugawara, T., Baskaran, V., Tsuzuki, W., and Nagao, A., (2002). Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by Caco-2 human intestinal cells and mice. J. Nutr. 132:946–951.
69. Sugawara, T., Kushiro, M., Zhang, H., Nara, E., Ono, H., and Nagao, A., (2001). Lysophosphatidylcholine enhances carotenoid uptake from mixed micelles by Caco-2 human intestinal cells. J. Nutr. 131:2921–2927.
70. Sugawara, T., Yamashita, K., Sakai, S., Asai, A., Nagao, A., Shiraishi, T., Hirata, T., (2007). Induction of apoptosis in DLD-1 human colon cancer cells by peridinin isolated from the dinoflagellate, Heterocapsa triquetra. Biosci. Biotechnol. Biochem. 71:1069–1072.
71. Tanaka, T., Kawamori, T., Ohnishi, M., Makita, H., Mori, H., Satoh, K., and Hara, A., (1995). Suppression of azoxymethane-induced rat colon carcinogenesis by dietary administration of naturally occurring xanthophylls astaxanthin and canthaxanthin during the postinitiation phase. Carcinogenesis. 16:2957–2963.
72. Tanaka, T., Makita, H., Ohnishi, M., Mori, H., Satoh, K., and Hara, A., (1995). Chemoprevention of rat oral carcinogenesis by naturally occurring xanthophylls, astaxanthin and canthaxanthin. Cancer Res. 55:4059–4064.
73. Tanaka, T., Morishita, Y., Suzui, M., Kojima, T., Okumura, A., and Mori, H., (1994). Chemoprevention of mouse urinary bladder carcinogenesis by the naturally occurring carotenoid astaxanthin. Carcinogenesis. 15:15–19.
74. Tsukui, T., Konno, K., Hosokawa, M., Maeda, H., Sashima, T., and Miyashita, K., (2007). Fucoxanthin and fucoxanthinol enhance the amount of docosahexaenoic acid in the liver of KKAy obese/diabetic mice. J. Agric. Food Chem. 55:5025–5029.
75. Yoshida, H., Yanai, H., Ito, K., Tomono, Y., Koikeda, T., Tsukahara, H., and Tada, N., (2010). Administration of natural astaxanthin increases serum HDL-cholesterol and adiponectin in subjects with mild hyperlipidemia. Atherosclerosis. 209:520–523.
76. Yoshida, T., Maoka, T., Das, S. K., Kanazawa, K., Horinaka, M., Wakada, M., Sakai, T., (2007). Halocynthiaxanthin and peridinin sensitize colon cancer cell lines to tumor necrosis factor-related apoptosis-inducing ligand. Mol. Cancer Res. 5:615–625.
77. Zhang, Z., Zhang, P., Hamada, M., Takahashi, S., Xing, G., Liu, J., and Sugiura, N., (2008). Potential chemoprevention effect of dietary fucoxanthin on urinary bladder cancer EJ-1 cell line. Oncol. Rep. 20:1099–1103.