Absorption and metabolism of xanthophylls

Marine Drugs

Volumn 9, Issue 6, 2011, Pages 1024-1037

  Kotake Nara, Eiichi ^a   Nagao, Akihiko ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

Absorption; Bioavailability; Carotenoid; Metabolism; Xanthophyll

Indexed keywords

BETA CAROTENE EPOXIDE; CAPSANTHIN 5,6 EPOXIDE; CAROTENOID; FUCOXANTHIN; LUTEIN 5,6 EPOXIDE; NEOXANTHIN; UNCLASSIFIED DRUG; VIOLAXANTHIN; XANTHOPHYLL;

BIOAVAILABILITY; CHEMICAL STRUCTURE; DIETARY INTAKE; DIFFUSION; ENZYME METABOLISM; EXCRETION; HUMAN; INTESTINE ABSORPTION; INTESTINE EPITHELIUM; METABOLISM; METABOLITE; NONHUMAN; REVIEW;

MAMMALIA;

EID: 79959722595     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md9061024     Document Type: Review

References (76)

1. Miller, N.J.; Sampson, J.; Candeias, L.P.; Bramley, P.M.; Rice-Evans, C.A. Antioxidant activities of carotenes and xanthophylls. FEBS Lett. 1996, 384, 240-242. (Pubitemid 26125229)
2. Di Mascio, P.; Kaiser, S.; Sies, H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys. 1989, 274, 532-538. (Pubitemid 19261144)
3. Junghans, A.; Sies, H.; Stahl, W. Macular pigments lutein and zeaxanthin as blue light filters studied in liposomes. Arch. Biochem. Biophys. 2001, 391, 160-164. (Pubitemid 32662257)
4. Katsuura, S.; Imamura, T.; Bando, N.; Yamanishi, R. Beta-carotene and beta-cryptoxanthin but not lutein evoke redox and immune changes in RAW264 murine macrophages. Mol. Nutr. Food Res. 2009, 53, 1396-1405.
5. Yamaguchi, M.; Weitzmann, M.N. The bone anabolic carotenoid beta-cryptoxanthin enhances transforming growth factor-beta1-induced SMAD activation in MC3T3 preosteoblasts. Int. J. Mol. Med. 2009, 24, 671-675.
6. Uchiyama, S.; Yamaguchi, M. Oral administration of beta-cryptoxanthin prevents bone loss in ovariectomized rats. Int. J. Mol. Med. 2006, 17, 15-20.
7. Aizawa, K.; Inakuma, T. Dietary capsanthin, the main carotenoid in paprika (Capsicum annuum), alters plasma high-density lipoprotein-cholesterol levels and hepatic gene expression in rats. Br. J. Nutr. 2009, 102, 1760-1766.
8. Hussein, G.; Sankawa, U.; Goto, H.; Matsumoto, K.; Watanabe, H. Astaxanthin, a carotenoid with potential in human health and nutrition. J. Nat. Prod. 2006, 69, 443-449.
9. Yuan, J.P.; Peng, J.; Yin, K.; Wang, J.H. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol. Nutr. Food Res. 2011, 55, 150-165.
10. Okuzumi, J.; Nishino, H.; Murakoshi, M.; Iwashima, A.; Tanaka, Y.; Yamane, T.; Fujita, Y.; Takahashi, T. Inhibitory effects of fucoxanthin, a natural carotenoid, on n-myc expression and cell cycle progression in human malignant tumor cells. Cancer Lett. 1990, 55, 75-81.
11. Hosokawa, M.; Wanezaki, S.; Miyauchi, K.; Kurihara, H.; Kohno, H.; Kawabata, J.; Odashima, S.; Takahashi, K. Apoptosis-inducing effect of fucoxanthin on human leukemia cell line HL-60. Food Sci. Technol. Res. 1999, 5, 243-246. (Pubitemid 129607585)
12. Kotake-Nara, E.; Terasaki, M.; Nagao, A. Characterization of apoptosis induced by fucoxanthin in human promyelocytic leukemia cells. Biosci. Biotechnol. Biochem. 2005, 69, 224-227. (Pubitemid 40383507)
13. Kotake-Nara, E.; Kushiro, M.; Zhang, H.; Sugawara, T.; Miyashita, K.; Nagao, A. Carotenoids affect proliferation of human prostate cancer cells. J. Nutr. 2001, 131, 3303-3306. (Pubitemid 33136153)
14. Kotake-Nara, E.; Sugawara, T.; Nagao, A. Antiproliferative effect of neoxanthin and fucoxanthin on cultured cells. Fish. Sci. 2005, 71, 459-461. (Pubitemid 40689911)
15. Okuzumi, J.; Takahashi, T.; Yamane, T.; Kitao, Y.; Inagake, M.; Ohya, K.; Nishino, H.; Tanaka, Y. Inhibitory effects of fucoxanthin, a natural carotenoid, on N-ethyl-N′-nitro-N-nitrosoguanidine-induced mouse duodenal carcinogenesis. Cancer Lett. 1993, 68, 159-168. (Pubitemid 23090674)
16. Sakai, S.; Sugawara, T.; Matsubara, K.; Hirata, T. Inhibitory effect of carotenoids on the degranulation of mast cells via suppression of antigen-induced aggregation of high affinity IgE receptors. J. Biol. Chem. 2009, 284, 28172-28179.
17. Maeda, H.; Hosokawa, M.; Sashima, T.; Miyashita, K. 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. 2007, 55, 7701-7706. (Pubitemid 47522175)
18. Khachik, F.; Beecher, G.R.; Goli, M.B.; Lusby, W.R. Separation, identification, and quantification of carotenoids in fruits, vegetables and human plasma by high performance liquid chromatography. Pure Appl. Chem. 1991, 63, 71-90.
19. Khachik, F.; Spangler, C.J.; Smith, J.C., Jr.; Canfield, L.M.; Steck, A.; Pfander, H. Identification, quantification, and relative concentrations of carotenoids and their metabolites in human milk and serum. Anal. Chem. 1997, 69, 1873-1881.
20. Slifka, K.A.; Bowen, P.E.; Stacewicz-Sapuntzakis, M.; Crissey, S.D. A survey of serum and dietary carotenoids in captive wild animals. J. Nutr. 1999, 129, 380-390. (Pubitemid 29072125)
21. Richelle, M.; Enslen, M.; Hager, C.; Groux, M.; Tavazzi, I.; Godin, J.P.; Berger, A.; Métairon, S.; Quaile, S.; Piguet-Welsch, C.; et al. Both free and esterified plant sterols reduce cholesterol absorption and the bioavailability of beta-carotene and alpha-tocopherol in normocholesterolemic humans. Am. J. Clin. Nutr. 2004, 80, 171-177. (Pubitemid 41115571)
22. Maiani, G.; Castón, M.J.; Catasta, G.; Toti, E.; Cambrodón, I.G.; Bysted, A.; Granado-Lorencio, F.; Olmedilla-Alonso, B.; Knuthsen, P.; Valoti, M.; et al. Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol. Nutr. Food Res. 2009, 53 (Suppl. 2), S194-S218.
23. Holst, B.; Williamson, G. Nutrients and phytochemicals: from bioavailability to bioefficacy beyond antioxidants. Curr. Opin. Biotechnol. 2008, 19, 73-82.
24. Zaripheh, S.; Erdman, J.W., Jr. Factors that influence the bioavailablity of xanthophylls. J. Nutr. 2002, 132, 531S-534S.
25. Yonekura, L.; Nagao, A. Intestinal absorption of dietary carotenoids. Mol. Nutr. Food Res. 2007, 51, 107-115. (Pubitemid 46144766)
26. Rock, C.L.; Lovalvo, J.L.; Emenhiser, C.; Ruffin, M.T.; Flatt, S.W.; Schwartz, S.J. Bioavailability of beta-carotene is lower in raw than in processed carrots and spinach in women. J. Nutr. 1998, 128, 913-916. (Pubitemid 28225526)
27. Small, D.M.; Penkett, S.A.; Chapman, D. Studies on simple and mixed bile salt micelles by nuclear magnetic resonance spectroscopy. Biochim. Biophys. Acta. 1969, 176, 178-189.
28. Yeum, K.J.; Russell, R.M. Carotenoid bioavailability and bioconversion. Annu. Rev. Nutr. 2002, 22, 483-504. (Pubitemid 35221470)
29. Hollander, D.; Ruble, P.E., Jr. Beta-carotene intestinal absorption: Bile, fatty acid, pH, and flow rate effects on transport. Am. J. Physiol. Endocrinol. Metab. 1978, 235, E686-E691.
30. Scita, G.; Aponte, G.W.; Wolf, G. Uptake and cleavage of β-carotene by cultures of rat small intestinal cells and human lung fibroblasts. J. Nutr. Biochem. 1992, 3, 118-123.
31. Sugawara, T.; Kushiro, M.; Zhang, H.; Nara, E.; Ono, H.; Nagao, A. Lysophosphatidylcholine enhances carotenoid uptake from mixed micelles by Caco-2 human intestinal cells. J. Nutr. 2001, 131, 2921-2927. (Pubitemid 33063124)
32. Sugawara, T.; Baskaran, V.; Tsuzuki, W.; Nagao, A. Brown algae fucoxanthin is hydrolyzed to fucoxanthinol during absorption by Caco-2 human intestinal cells and mice. J. Nutr. 2002, 132, 946-951. (Pubitemid 34493558)
33. Asai, A.; Sugawara, T.; Ono, H.; Nagao, A. Biotransformation of fucoxanthinol into amarouciaxanthin A in mice and HepG2 cells. Drug Metab. Dispos. 2004, 32, 205-211.
34. Asai, A.; Terasaki, M.; Nagao, A. An epoxide-furanoid rearrangement of spinach neoxanthin occurs in the gastrointestinal tract of mice and in vitro: Formation and cytostatic activity of neochrome stereoisomers. J. Nutr. 2004, 134, 2237-2243. (Pubitemid 39201591)
35. Sangeetha, R.K.; Bhaskar, N.; Divakar, S.; Baskaran, V. Bioavailability and metabolism of fucoxanthin in rats: structural characterization of metabolites by LC-MS (APCI). Mol. Cell. Biochem. 2010, 333, 299-310.
36. Baskaran, V.; Sugawara, T.; Nagao, A. Phospholipids affect the intestinal absorption of carotenoids in mice. Lipids 2003, 38, 705-711. (Pubitemid 37362262)
37. Matsuno, T.; Ookubo, M. A new carotenoid, halocynthiaxanthin from the sea squirt, Halocynthia Roretzi. Tetrahedron Lett. 1981, 22, 4659-4660. (Pubitemid 12208567)
38. Matsuno, T.; Ookubo, M.; Komori, T. Carotenoids of tunicates, III. The structural elucidation of two new marine carotenoids, amarouciaxanthin A and B. J. Nat. Prod. 1985, 48, 606-613.
39. Strand, A.; Herstad, O.; Liaaen-Jensen, S. Fucoxanthin metabolites in egg yolks of laying hens. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1998, 119, 963-974. (Pubitemid 28389208)
40. Matsuno, T.; Ohkubo, M.; Toriiminami, Y.; Tsushima, M.; Sakaguchi, S.; Minami, T.; Maoka, T. Carotenoids in food chain between freshwater fish and aquatic insects. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1999, 124, 341-345. (Pubitemid 29502600)
41. Asai, A.; Yonekura, L.; Nagao, A. Low bioavailability of dietary epoxyxanthophylls in humans. Br. J. Nutr. 2008, 100, 273-277.
42. Yonekura, L.; Nagao, A. Soluble fibers inhibit carotenoid micellization in vitro and uptake by Caco-2 cells. Biosci. Biotechnol. Biochem. 2009, 73, 196-199.
43. Pérez-Gálvez, A.; Martin, H.D.; Sies, H.; Stahl, W. Incorporation of carotenoids from paprika oleoresin into human chylomicrons. Br. J. Nutr. 2003, 89, 787-793. (Pubitemid 36798254)
44. Barua, A.B.; Olson, J.A. Xanthophyll epoxides, unlike beta-carotene monoepoxides, are not detectibly absorbed by humans. J. Nutr. 2001, 131, 3212-3215. (Pubitemid 33136137)
45. Barua, A.B. Intestinal absorption of epoxy-beta-carotenes by humans. Biochem. J. 1999, 339 (Pt. 2), 359-362.
46. Reboul, E.; Abou, L.; Mikail, C.; Ghiringhelli, O.; André, M.; Portugal, H.; Jourdheuil-Rahmani, D.; Amiot, M.J.; Lairon, D.; Borel, P. Lutein transport by Caco-2 TC-7 cells occurs partly by a facilitated process involving the scavenger receptor class B type I (SR-BI). Biochem. J. 2005, 387 (Pt. 2), 455-461. (Pubitemid 40571232)
47. Kiefer, C.; Sumser, E.; Wernet, M.F.; Von Lintig, J. A Class B scavenger receptor mediates the cellular uptake of carotenoids in Drosophila. Proc. Natl. Acad. Sci. USA 2002, 99, 10581-10586.
48. Borel, P.; Moussa, M.; Reboul, E.; Lyan, B.; Defoort, C.; Vincent-Baudry, S.; Maillot, M.; Gastaldi, M.; Darmon, M.; Portugal, H.; et al. Human plasma levels of vitamin E and carotenoids are associated with genetic polymorphisms in genes involved in lipid metabolism. J. Nutr. 2007, 137, 2653-2659.
49. Moussa, M.; Landrier, J.F.; Reboul, E.; Ghiringhelli, O.; Coméra, C.; Collet, X.; Fröhlich, K.; Böhm, V.; Borel, P. Lycopene absorption in human intestinal cells and in mice involves scavenger receptor class B type I but not Niemann-Pick C1-Like 1. J. Nutr. 2008, 138, 1432-1436.
50. O'Sullivan, L.; Aisling, S.A.; O'Brien, N.M. Investigation of beta-carotene and lutein transport in Caco-2 cells: carotenoid-carotenoid interactions and transport inhibition by ezetimibe. Int. J. Vitam. Nutr. Res. 2009, 79, 337-347.
51. During, A.; Hussain, M.M.; Morel, D.W.; Harrison, E.H. Carotenoid uptake and secretion by CaCo-2 cells: Beta-carotene isomer selectivity and carotenoid interactions. J. Lipid Res. 2002, 43, 1086-1095. (Pubitemid 34760880)
52. During, A.; Harrison, E.H. Mechanisms of provitamin A (carotenoid) and vitamin A (retinol) transport into and out of intestinal Caco-2 cells. J. Lipid Res. 2007, 48, 2283-2294. (Pubitemid 47529570)
53. During, A.; Dawson, H.D.; Harrison, E.H. Carotenoid transport is decreased and expression of the lipid transporters SR-BI, NPC1L1, and ABCA1 is downregulated in Caco-2 cells treated with ezetimibe. J. Nutr. 2005, 135, 2305-2312. (Pubitemid 41429582)
54. van Bennekum, A.; Werder, M.; Thuahnai, S.T.; Han, C.H.; Duong, P.; Williams, D.L.; Wettstein, P.; Schulthess, G.; Phillips, M.C.; Hauser, H. Class B scavenger receptor-mediated intestinal absorption of dietary beta-carotene and cholesterol. Biochemistry 2005, 44, 4517-4525. (Pubitemid 40403994)
55. Lobo, G.P.; Hessel, S.; Eichinger, A.; Noy, N.; Moise, A.R.; Wyss, A.; Palczewski, K.; von Lintig, J. ISX is a retinoic acid-sensitive gatekeeper that controls intestinal beta, beta-carotene absorption and vitamin A production. FASEB J. 2010, 24, 1656-1666.
56. Fransen, H.P.; de Jong, N.; Wolfs, M.; Verhagen, H.; Verschuren, W.M.; Lütjohann, D.; von Bergmann, K.; Plat, J.; Mensink, R.P. Customary use of plant sterol and plant stanol enriched margarine is associated with changes in serum plant sterol and stanol concentrations in humans. J. Nutr. 2007, 137, 1301-1306. (Pubitemid 46701926)
57. Yu, L.; von Bergmann, K.; Lutjohann, D.; Hobbs, H.H.; Cohen, J.C. Selective sterol accumulation in ABCG5/ABCG8-deficient mice. J. Lipid Res. 2004, 45, 301-307. (Pubitemid 38228828)
58. Herron, K.L.; McGrane, M.M.; Waters, D.; Lofgren, I.E.; Clark, R.M.; Ordovas, J.M.; Fernandez, M.L. The ABCG5 polymorphism contributes to individual responses to dietary cholesterol and carotenoids in Eggs. J. Nutr. 2006, 136, 1161-1165.
59. Shen, J.; Cross, S.T.; Tang-Liu, D.D.; Welty, D.F. Evaluation of an immortalized retinal endothelial cell line as an in vitro model for drug transport studies across the blood-retinal barrier. Pharm. Res. 2003, 20, 1357-1363. (Pubitemid 37164042)
60. Gyémánt, N.; Tanaka, M.; Molnár, P.; Deli, J.; Mándoky, L.; Molnár, J. Reversal of multidrug resistance of cancer cells in vitro: modification of drug resistance by selected carotenoids. Anticancer Res. 2006, 26, 367-374. (Pubitemid 43206100)
61. Molnár, J.; Gyémánt, N.; Mucsi, I.; Molnár, A.; Szabó, M.; Körtvélyesi, T.; Varga, A.; Molnár, P.; Tóth, G. Modulation of multidrug resistance and apoptosis of cancer cells by selected carotenoids. In Vivo 2004, 18, 237-244. (Pubitemid 38489008)
62. Ugocsai, K.; Varga, A.; Molnár, P.; Antus, S.; Molnár, J. Effects of selected flavonoids and carotenoids on drug accumulation and apoptosis induction in multidrug-resistant colon cancer cells expressing MDR1/LRP. In Vivo 2005, 19, 433-438. (Pubitemid 40467630)
63. Khachik, F.; Bernstein, P.S.; Garland, D.L. Identification of lutein and zeaxanthin oxidation products in human and monkey retinas. Invest. Ophthalmol. Vis. Sci. 1997, 38, 1802-1811.
64. Khachik, F.; de Moura, F.F.; Zhao, D.Y.; Aebischer, C.P.; Bernstein, P.S. Transformations of selected carotenoids in plasma, liver, and ocular tissues of humans and in nonprimate animal models. Invest. Ophthalmol. Vis. Sci. 2002, 43, 3383-3392. (Pubitemid 35334344)
65. Bhosale, P.; Bernstein, P.S. Quantitative measurement of 3′-oxolutein from human retina by normal-phase high-performance liquid chromatography coupled to atmospheric pressure chemical ionization mass spectrometry. Anal. Biochem. 2005, 345, 296-301. (Pubitemid 41375959)
66. Bhosale, P.; Zhao, D.Y.; Serban, B.; Bernstein, P.S. Identification of 3-methoxyzeaxanthin as a novel age-related carotenoid metabolite in the human macula. Invest. Ophthalmol. Vis. Sci. 2007, 48, 1435-1440. (Pubitemid 351261322)
67. Yonekura, L.; Kobayashi, M.; Terasaki, M.; Nagao, A. Keto-carotenoids are the major metabolites of dietary lutein and fucoxanthin in mouse tissues, J. Nutr. 2010, 140, 1824-1831.
68. Etoh, H.; Utsunomiya, Y.; Komori, A.; Murakami, Y.; Oshima, S.; Inakuma, T. Carotenoids in human blood plasma after ingesting paprika juice. Biosci. Biotechnol. Biochem. 2000, 64, 1096-1098.
69. Zeng, S.; Furr, H.C.; Olson, J.A. Metabolism of carotenoid analogs in humans. Am. J. Clin. Nutr. 1992, 56, 433-439.
70. Khachik, F. An efficient conversion of (3R,3′R,6′R)-lutein to (3R,3′S,6′R)-lutein (3′-epilutein) and (3R,3′R)- zeaxanthin. J. Nat. Prod. 2003, 66, 67-72.
71. Khachik, F.; Englert, G.; Beecher, G.R.; Smith, J.C., Jr. Isolation, structural elucidation, and partial synthesis of lutein dehydration products in extracts from human plasma. J. Chromatogr. B Biomed. Appl. 1995, 670, 219-233.
72. Kiefer, C.; Hessel, S.; Lampert, J.M.; Vogt, K.; Lederer, M.O.; Breithaupt, D.E.; von Lintig, J. Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J. Biol. Chem. 2001, 276, 14110-14116.
73. Hu, K.Q.; Liu, C.; Ernst, H.; Krinsky, N.I.; Russell, R.M.; Wang, X.D. The biochemical characterization of ferret carotene-9′,10′- monooxygenase catalyzing cleavage of carotenoids in vitro and in vivo. J. Biol. Chem. 2006, 281, 19327-19338.
74. Mein, J.R.; Dolnikowski, G.G.; Ernst, H.; Russell, R.M.; Wang, X.D. Enzymatic formation of apo-carotenoids from the xanthophyll carotenoids lutein, zeaxanthin and β-cryptoxanthin by ferret carotene-9′,10′- monooxygenase. Arch. Biochem. Biophys. 2011, 506, 109-121.
75. Våge, D.I.; Boman, I.A. A nonsense mutation in the beta-carotene oxygenase 2 (BCO2) gene is tightly associated with accumulation of carotenoids in adipose tissue in sheep (Ovis aries). BMC Genet. 2010, 11, 10.
76. Amengual, J.; Lobo, G.P.; Golczak, M.; Li, H.N.; Klimova, T.; Hoppel, C.L.; Wyss, A.; Palczewski, K.; von Lintig, J. A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J. 2011, 25, 948-959.