Xanthophylls are preferentially taken up compared with β-carotene by retinal cells via a SRBI-dependent mechanism

Journal of Lipid Research

Volumn 49, Issue 8, 2008, Pages 1715-1724

  During, Alexandrine ^a,b   Doraiswamy, Sundari ^a   Harrison, Earl H ^a,c  

^a BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

ARPE 19 cells; Carotenoids; Cellular uptake; Scavenger receptor class B type I; Small interfering RNAs; Xanthophylls

Indexed keywords

BETA CAROTENE; BETA CAROTENE 15,15' MONOOXYGENASE; RETINOL; SCAVENGER RECEPTOR BI; SMALL INTERFERING RNA; XANTHOPHYLL; ZEAXANTHIN; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B;

ARTICLE; CELL DIFFERENTIATION; CELL TRANSPORT; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG SELECTIVITY; DRUG TRANSPORT; DRUG UPTAKE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CELL; RETINA MACULA LUTEA; CELL CULTURE; CYTOLOGY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BETA CAROTENE; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; LUTEIN; PIGMENT EPITHELIUM OF EYE; SCAVENGER RECEPTORS, CLASS B; XANTHOPHYLLS;

EID: 51449101273     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M700580-JLR200     Document Type: Article

References (51)

1. Moeller, S. M., N. Parekh, L. Tinker, C. Ritenbaugh, B. Blodi, R. B. Wallace, and J. A. Mares. 2006. Associations between intermediate age-related macular degeneration and lutein and zeaxanthin in the Carotenoids in Age-Related Eye Disease Study (CAREDS): ancillary study of the Women's Health Initiative. Arch. Ophthalmol. 124: 1151-1162.
2. Snodderly, D. M. 1995. Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. Am. J. Clin. Nutr. 62 (6Suppl.): 1448S-1461S.
3. Mozaffarieh, M., S. Sacu, and A. Wedrich. 2003. The role of the carotenoids, lutein and zeaxanthin, in protecting against agerelated macular degeneration: a review based on controversial evidence. Nutr. J. 11: 20-28.
4. Parker, R. S. 1989. Carotenoids in human blood and tissues. J. Nutr. 119: 101-104.
5. Goodwin, T. W., and G. Britton. 1988. Distribution and analysis of carotenoids. In Plant Pigments, T.W. Goodwin, editor. Academic Press, New York. 61-127.
6. Holden, J. M., A. L. Eldridge, G. R. Beecher, M. I. Buzzard, S. Bhagwat, C. S. Davis, L. W. Douglass, S. Gebhardt, D. Haytowitz, and S. Schakel. 1999. Carotenoid content of US foods: an update of the database. J. Food Compos. Anal. 12: 169-196.
7. Curran-Celentano, J., B. R. Hammond, Jr., T. A. Ciulla, D. A. Cooper, L. M. Pratt, and R. B. Danis. 2001. Relation between dietary intake, serum concentrations, and retinal concentrations of lutein and zeaxanthin in adults in a Midwest population. Am. J. Clin. Nutr. 74: 796-802.
8. Broekmans, W. M., I. A. Klopping-Ketelaars, C. R. Schuurman, H. Verhagen, H. van den Berg, F. J. Kok, and G. van Poppel. 2002. Fruits and vegetables increase plasma carotenoids and vitamins and decrease homocysteine in humans. J. Nutr. 130: 1578-1583.
9. Stacewicz-Sapuntzakis, M., P. E. Bowen, and J. A. Mares-Perlman. 1993. Serum reference values for lutein and zeaxanthin using a rapid separation technique. Ann. N. Y. Acad. Sci. 691: 207-209.
10. Handelman, G. J., D. M. Snodderly, A. J. Adler, M. D. Russett, and E. A. Dratz. 1992. Measurement of carotenoids in human and monkey retinas. Methods Enzymol. 213: 220-230.
11. Schmitz, H. H., C. L. Poor, E. T. Gugger, and J. W. Erdman, Jr. 1993. Analysis of carotenoids in human and animal tissues. Methods Enzymol. 214: 102-116.
12. Bone, R. A., J. T. Landrum, and S. L. Tarsis. 1985. Preliminary identification of the human macular pigment. Vision Res. 25: 1531-1535.
13. Handelman, G. J., E. A. Dratz, C. C. Reay, and J. G. van Kuijk. 1988. Carotenoids in the human macula and whole retina. Invest. Ophthalmol. Vis. Sci. 29: 850-855.
14. Landrum, J. T., R. A. Bone, L. L. Moore, and C. M. Gomez. 1999. Analysis of zeaxanthin distribution within individual human retinas. Methods Enzymol. 299: 457-467.
15. The Eye Disease Case-Control Study Group. 1992. Risk factors for neovascular age-related macular degeneration. Arch. Ophthalmol. 110: 1701-1708.
16. Bone, R. A., J. T. Landrum, Z. Dixon, Y. Chen, and C. M. Llerena. 2000. Lutein and zeaxanthin in the eyes, serum and diet of human subjects. Exp. Eye Res. 71: 239-245.
17. Schalch, W., W. Cohn, F. M. Barker, W. Kopcke, J. Mellerio, A. C. Bird, A. G. Robson, F. F. Fitzke, and F. J. van Kuijk. 2007. Xanthophyll accumulation in the human retina during supplementation with lutein or zeaxanthin - the LUXEA (LUtein Xanthophyll Eye Accumulation) study. Arch. Biochem. Biophys. 458: 128-135.
18. Haegerstrom-Portnoy, G. 1988. Short-wavelength-sensitive-cone sensitivity loss with aging: a protective role for macular pigment? J. Opt. Soc. Am. A. 5: 2140-2144.
19. Schalch, W. 1992. Carotenoids in the retina-a review of their possible role in preventing or limiting damage caused by light and oxygen. EXS. 62: 280-298.
20. Sperling, H. G., C. Johnson, and R. S. Harwerth. 1980. Differential spectral photic damage to primate cones. Vision Res. 20: 1117-1125.
21. Reading, V. M., and R. A. Weale. 1974. Macular pigment and chromatic aberration. J. Opt. Soc. Am. 64: 231-234.
22. Chucair, A. J., N. P. Rotstein, J. P. SanGiovanni, A. During, E. Y. Chew, and L. E. Politi. 2007. Lutein and zeaxanthin protect photoreceptors from apoptosis induced by oxidative stress. Relation with docosahexaenoic acid. Invest. Ophthalmol. Vis. Sci. 48: 5168-5177.
23. Saari, J. C. 2000. Biochemistry of visual pigment regeneration. Invest. Ophthalmol. Vis. Sci. 41: 337-348.
24. Kawaguchi, R., J. Yu, J. Honda, J. Hu, J. Whitelegge, P. Ping, P. Wiita, D. Bok, and H. Sun. 2007. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science. 315: 820-825.
25. Yemelyanov, A. Y., N. B. Katz, and P. S. Bernstein. 2001. Ligandbinding characterization of xanthophyll carotenoids to solubilized membrane proteins derived from human retina. Exp. Eye Res. 72: 381-392.
26. Reboul, E., L. Abou, C. Mikail, O. Ghiringhelli, M. Andre, H. Portugal, D. Jourdheuil-Rahmani, M. J. Amiot, D. Lairon, and P. Borel. 2005. 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. 387: 455-461.
27. During, A., H. D. Dawson, and E. H. Harrison. 2005. 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. 135: 2305-2312.
28. Van Bennekum, A., M. Werder, S. T. Thuahnai, C. H. Han, P. Duong, D. L. Williams, P. Wettstein, G. Schulthess, M. C. Phillips, and H. Hauser. 2005. Class B scavenger receptor-mediated intestinal absorption of dietary beta-carotene and cholesterol. Biochemistry. 44: 4517-4525.
29. Kiefer, C., E. Sumser, M. F. Wernet, and J. Von Lintig. 2002. A class B scavenger receptor mediates the cellular uptake of carotenoids in Drosophila. Proc. Natl. Acad. Sci. USA. 99: 10581-10586.
30. Dunn, K. C., A. E. Aotaki-Keen, F. R. Putkey, and L. M. Hjelmeland. 1996. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62: 155-169.
31. During, A., M. M. Hussain, D. W. Morel, and E. H. Harrison. 2002. Carotenoid uptake and secretion by CaCo-2 cells: beta-carotene isomer selectivity and carotenoid interactions. J. Lipid Res. 43: 1086-1095.
32. During, A., G. Albaugh, and J. C. Smith. 1998. Characterization of β-carotene 15,15′-dioxygenase activity in TC7 clone of human intestinal cell line Caco-2. Biochem. Biophys. Res. Commun. 249: 467-474.
33. During, A., A. Nagao, C. Hoshino, and J. Terao. 1996. Assay of bcarotene 15,15′-dioxygenase activity by reverse-phase high-pressure liquid chromatography. Anal. Biochem. 241: 199-205.
34. Barua, A. B., and J. A. Olson. 1998. Reversed-phase gradient highperformance liquid chromatographic procedure for simultaneous analysis of very polar to nonpolar retinoids, carotenoids and tocopherols in animal and plant samples. J. Chromatogr. B Biomed. Sci. Appl. 707: 69-79.
35. Barua, A. B., D. Kostic, and J. A. Olson. 1993. New simplified procedures for the extraction and simultaneous high-performance liquid chromatographic analysis of retinol, tocopherols and carotenoids in human serum. J. Chromatogr. 617: 257-264.
36. Aman, R., J. Biehl, R. Carle, J. Conrad, U. Beifuss, and A. Schieber. 2005. Application of HPLC coupled with DAD, APcI-MS and NMR to the analysis of lutein and zeaxanthin stereoisomers in thermally processed vegetables. Food Chem. 92: 753-763.
37. Khachik, F., C. J. Spangler, J. C. Smith, Jr., L. M. Canfield, A. Steck, and H. Pfander. 1997. Identification, quantification, and relative concentrations of carotenoids and their metabolites in human milk and serum. Anal. Chem. 69: 1873-1881.
38. Janssen, J. J., E. D. Kuhlmann, A. H. van Vugt, H. J. Winkens, B. P. Janssen, A. F. Deutman, and C. A. Driessen. 2000. Retinoic acid delays transcription of human retinal pigment neuroepithelium marker genes in ARPE-19 cells. Neuroreport. 11: 1571-1579.
39. Lornejad-Schäfer, M. R., C. Lambert, D. E. Breithaupt, H. K. Biesalski, and J. Frank. 2007. Solubility, uptake and biocompatibility of lutein and zeaxanthin delivered to cultured human retinal pigment epithelial cells in tween40 micelles. Eur. J. Nutr. 46: 79-86.
40. Bhatti, R. A., S. Yu, A. Boulanger, R. N. Fariss, Y. Guo, S. L. Bernstein, S. Gentleman, and T. M. Redmond. 2003. Expression of b-carotene 15,15′ monooxygenase in retina and RPE-choroid. Invest. Ophthalmol. Vis. Sci. 44: 44-49.
41. Ryeom, S. W., J. R. Sparrow, and R. L. Silverstein. 1996. CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J. Cell Sci. 109: 387-395.
42. Duncan, K. G., K. R. Bailey, J. P. Kane, and D. M. Schwartz. 2002. Human retinal pigment epithelial cells express scavenger receptors BI and BII. Biochem. Biophys. Res. Commun. 292: 1017-1022.
43. During, A., and E. H. Harrison. 2007. Mechanisms of provitamin A (carotenoid) and vitamin A (retinol) transport into and out of intestinal Caco-2 cells. J. Lipid Res. 48: 2283-2294.
44. Bernstein, P. S., N. A. Balashov, E. D. Tsong, and R. R. Rando. 1997. Retinal tubulin binds macular carotenoids. Invest. Ophthalmol. Vis. Sci. 38: 167-175.
45. Bhosale, P., A. J. Larson, J. M. Frederick, K. Southwick, C. D. Thulin, and P. S. Bernstein. 2004. Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1) as a zeaxanthinbinding protein in the macula of the human eye. J. Biol. Chem. 279: 49447-49454.
46. Tserentsoodol, N., N. V. Gordiyenko, I. Pascual, J. W. Lee, S. J. Fliesler, and I. R. Rodriguez. 2006. Intraretinal lipid transport is dependent on high density lipoprotein-like particle and class B scavenger receptors. Mol. Vis. 12: 1319-1333.
47. Yan, W., G. F. Jang, F. Haeseleer, N. Esumi, J. Chang, M. Kerrigan, M. Campochiaro, P. Campochiaro, K. Palczewski, and D. J. Zack. 2001. Cloning and characterization of a human β,β-carotene-15,15′-dioxygenase that is highly expressed in the retinal pigment epithelium. Genomics. 72: 193-202.
48. Chichili, G. R., D. Nohr, M. Schäffer, J. von Lintig, and H. K. Biesalski. 2005. β-Carotene conversion into vitamin A in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 46: 3562-3569.
49. Christen, W. G., J. E. Manson, R. J. Glynn, J. M. Gaziano, E. Y. Chew, J. E. Buring, and C. H. Hennekens. 2007. Beta carotene supplementation and age-related maculopathy in a randomized trial of US physicians. Arch. Ophthalmol. 125: 333-339.
50. Tserentsoodol, N., J. Sztein, M. Campos, N. V. Gordiyenko, R. N. Fariss, J. W. Lee, S. J. Fliesler, and I. R. Rodriguez. 2006. Uptake of cholesterol by the retina occurs primarily via a low density lipoprotein receptor-mediated process. Mol. Vis. 12: 1306-1318.
51. Romanchick, J. E., D. W. Morel, and E. H. Harrison. 1995. Distributions of carotenoids and a-tocopherol among lipoproteins do not change when human plasma is incubated in vitro. J. Nutr. 125: 2610-2617.