Mechanisms of selective delivery of xanthophylls to retinal pigment epithelial cells by human lipoproteins

Journal of Lipid Research

Volumn 57, Issue 10, 2016, Pages 1865-1878

  Thomas, Sara E ^a   Harrison, Earl H ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Carotenoids; Dietary lipids; Eye; High density lipoprotein; Low density lipoprotein; Lutein; Retina; Scavenger receptors; Transport; Zeaxanthin

Indexed keywords

BETA CAROTENE; HIGH DENSITY LIPOPROTEIN; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESO ZEAXANTHIN; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; XANTHOPHYLL; ZEAXANTHIN; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B;

ARTICLE; BINDING AFFINITY; BIOACCUMULATION; CELL DIFFERENTIATION; CELL METABOLISM; CELLULAR DISTRIBUTION; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EPITHELIUM CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; RETINAL PIGMENT EPITHELIUM; VITAMIN METABOLISM; ACTIVE TRANSPORT; CELL LINE; CYTOLOGY; METABOLISM; PHYSIOLOGY;

BETA CAROTENE; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; HUMANS; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; LUTEIN; RETINAL PIGMENT EPITHELIUM; SCAVENGER RECEPTORS, CLASS B; ZEAXANTHINS;

EID: 84990913648     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M070193     Document Type: Article

References (65)

1. Zarbin, M. A., and P. Rosenfeld. 2010. Pathway-based therapies for age-related macular degeneration: an integrated survey of emerging treatment alternatives. Retina. 30:1350-1367.
2. Wong, W. L., X. Su, X. Li, C. M. Cheung, R. Klein, C. Y. Cheng, and T. Y. Wong. 2014. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet. 2:e106-e116.
3. Kotake-Nara, E., and A. Nagao. 2011. Absorption and metabolism of xanthophylls. Mar. Drugs. 9:1024-1037.
4. Reboul, E., and P. Borel. 2011. Proteins involved in uptake, intracellular transport and basolateral secretion of fat-soluble vitamins and carotenoids by mammalian enterocytes. Prog. Lipid Res. 50:388-402.
5. Namitha, K. K., and P. Negi. 2010. Chemistry and biotechnology of carotenoids. Crit. Rev. Food Sci. Nutr. 50:728-760.
6. Brevik, A., L. F. Andersen, A. Karlsen, K. U. Trygg, R. Blomhoff, and C. A. Drevon. 2004. Six carotenoids in plasma used to assess recommended intake of fruits and vegetables in a controlled feeding study. Eur. J. Clin. Nutr. 58:1166-1173.
7. Chung, H. Y., A. L. Ferreira, S. Epstein, S. A. Paiva, C. Castaneda-Sceppa, and E. J. Johnson. 2009. Site-specific concentrations of carotenoids in adipose tissue: relations with dietary and serum carotenoid concentrations in healthy adults. Am. J. Clin. Nutr. 90:533-539.
8. Peng, Y. M., Y. S. Peng, Y. Lin, T. Moon, D. J. Roe, and C. Ritenbaugh. 1995. Concentrations and plasma-tissue-diet relationships of carotenoids, retinoids, and tocopherols in humans. Nutr. Cancer. 23:233-246.
9. Bone, R. A., J. T. Landrum, L. M. Friedes, C. M. Gomez, M. D. Kilburn, E. Menendez, I. Vidal, and W. Wang. 1997. Distribution of lutein and zeaxanthin stereoisomers in the human retina. Exp. Eye Res. 64:211-218.
10. Thomas, J. B., D. L. Duewer, I. O. Mugenya, K. W. Phinney, L. C. Sander, K. E. Sharpless, L. T. Sniegoski, S. S. Tai, M. J. Welch, and J. H. Yen. 2012. Preparation and value assignment of standard reference material 968e fat-soluble vitamins, carotenoids, and cholesterol in human serum. Anal. Bioanal. Chem. 402:749-762.
11. Schmitz, H. H., C. L. Poor, E. T. Gugger, and J. W. Erdman. 1993. Analysis of carotenoids in human and animal tissues. Methods Enzymol. 214:102-116.
12. Bone, R. A., J. T. Landrum, G. W. Hime, and A. Cains. 1993. Stereochemistry of the human macular carotenoids. Invest. Ophthalmol. Vis. Sci. 34:2033-2040.
13. Khachik, F., F. F. de Moura, D. Y. Zhao, C. P. Aebischer, and P. S. Bernstein. 2002. Transformations of selected carotenoids in plasma, liver, and ocular tissues of humans and in nonprimate animal models. Invest. Ophthalmol. Vis. Sci. 43:3383-3392.
14. Bernstein, P. S., B. Li, P. P. Vachali, A. Gorusupudi, R. Shyam, B. S. Henriksen, and J. M. Nolan. 2016. Lutein, zeaxanthin, and meso-zeaxanthin: the basic and clinical science underlying carotenoid-based nutritional interventions against ocular disease. Prog. Retin. Eye Res. 50:34-66.
15. Gorusupudi, A., R. Shyam, B. Li, P. Vachali, Y. K. Subhani, K. Nelson, and P. S. Bernstein. 2016. Developmentally regulated production of meso-zeaxanthin in chicken retinal pigment epithelium/choroid and retina. Invest. Ophthalmol. Vis. Sci. 57:1853-1861.
16. Johnson, E. J., M. Neuringer, R. M. Russell, W. Schalch, and D. M. Snodderly. 2005. Nutritional manipulation of primate retinas, III: Effects of lutein or zeaxanthin supplementation on adipose tissue and retina of xanthophyll-free monkeys. Invest. Ophthalmol. Vis. Sci. 46:692-702.
17. Thurnham, D. I., A. Tremel, and A. N. Howard. 2008. A supplementation study in human subjects with a combination of meso-zeaxanthin, (3R, 3'R)-zeaxanthin and (3R, 3'R, 6'R)-lutein. Br. J. Nutr. 100:1307-1314.
18. Bone, R. A., J. T. Landrum, Y. Cao, A. N. Howard, and F. Alvarez-Calderon. 2007. Macular pigment response to a supplement containing meso-zeaxanthin, lutein and zeaxanthin. Nutr. Metab. (Lond.). 4:12.
19. Fliesler, S. J., and L. Bretillon. 2010. The ins and outs of cholesterol in the vertebrate retina. J. Lipid Res. 51:3399-3413.
20. 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.
21. Akanuma, S., A. Yamamoto, S. Okayasu, M. Tachikawa, and K. Hosoya. 2009. High-density lipoprotein-associated alpha-tocopherol uptake by human retinal pigment epithelial cells (ARPE-19 cells): the irrelevance of scavenger receptor class B, type I. Biol. Pharm. Bull. 32:1131-1134.
22. Dunn, K. C., A. D. Marmorstein, V. L. Bonilha, E. Rodriguez-Boulan, F. Giordano, and L. M. Hjelmeland. 1998. Use of the ARPE-19 cell line as a model of RPE polarity: basolateral secretion of FGF5. Invest. Ophthalmol. Vis. Sci. 39:2744-2749.
23. During, A., S. Doraiswamy, and E. H. Harrison. 2008. Xanthophylls are preferentially taken up compared with beta-carotene by retinal cells via a SRBI-dependent mechanism. J. Lipid Res. 49:1715-1724.
24. Gordiyenko, N., M. Campos, J. W. Lee, R. N. Fariss, J. Sztein, and I. R. Rodriguez. 2004. RPE cells internalize low-density lipoprotein (LDL) and oxidized LDL (oxLDL) in large quantities in vitro and in vivo. Invest. Ophthalmol. Vis. Sci. 45:2822-2829.
25. Finnemann, S. C., and R. L. Silverstein. 2001. Differential roles of CD36 and alphavbeta5 integrin in photoreceptor phagocytosis by the retinal pigment epithelium. J. Exp. Med. 194:1289-1298.
26. 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 particles and class B scavenger receptors. Mol. Vis. 12:1319-1333.
27. 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.
28. Romanchik, J. E., D. W. Morel, and E. H. Harrison. 1995. Distributions of carotenoids and alpha-tocopherol among lipoproteins do not change when human plasma is incubated in vitro. J. Nutr. 125:2610-2617.
29. Romanchik, J. E., E. H. Harrison, and D. W. Morel. 1997. Addition of lutein, lycopene, or β-carotene to LDL or serum in vitro: Effects on carotenoid distribution, LDL composition, and LDL oxidation. J. Nutr. Biochem. 8:681-688.
30. Ford, T., J. Graham, and D. Rickwood. 1994. Iodixanol: A nonionic iso-osmotic centrifugation medium for the formation of self-generated gradients. Anal. Biochem. 220:360-366.
31. Graham, J. M., J. A. Higgins, T. Gillott, T. Taylor, J. Wilkinson, T. Ford, and D. Billington. 1996. A novel method for the rapid separation of plasma lipoproteins using self-generating gradients of iodixanol. Atherosclerosis. 124:125-135.
32. 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.
33. Barua, A. B. 2001. Improved normal-phase and reversed-phase gradient high-performance liquid chromatography procedures for the analysis of retinoids and carotenoids in human serum, plant and animal tissues. J. Chromatogr. A. 936:71-82.
34. 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.
35. Nieland, T. J., M. Penman, L. Dori, M. Krieger, and T. Kirchhausen. 2002. Discovery of chemical inhibitors of the selective transfer of lipids mediated by the HDL receptor SR-BI. Proc. Natl. Acad. Sci. USA. 99:15422-15427.
36. Moussa, M., J. F. Landrier, E. Reboul, O. Ghiringhelli, C. Comér, X. Collet, K. Fröhlich, V. Böhm, and P. Borel. 2008. 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. 138:1432-1436.
37. Reboul, E., L. Abou, C. Mikail, O. Ghiringhelli, M. André, 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.
38. Cai, L., M. C. de Beer, F. C. de Beer, and D. R. van der Westhuyzen. 2005. Serum amyloid A is a ligand for scavenger receptor class B type I and inhibits high density lipoprotein binding and selective lipid uptake. J. Biol. Chem. 280:2954-2961.
39. Krinsky, N. I., D. G. Cornwell, and J. L. Oncley. 1958. The transport of vitamin A and carotenoids in human plasma. Arch. Biochem. Biophys. 73:233-246.
40. Dela Sena, C., J. Sun, S. Narayanasamy, K. M. Riedl, Y. Yuan, R. W. Curley, S. J. Schwartz, and E. H. Harrison. 2016. Substrate specificity of purified recombinant chicken β-carotene 9, 10-oxygenase (BCO2). J. Biol. Chem. 291:14609-14619.
41. Bone, R. A., and J. T. Landrum. 2010. Dose-dependent response of serum lutein and macular pigment optical density to supplementation with lutein esters. Arch. Biochem. Biophys. 504:50-55.
42. Babitt, J., B. Trigatti, A. Rigotti, E. J. Smart, R. G. Anderson, S. Xu, and M. Krieger. 1997. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae. J. Biol. Chem. 272:13242-13249.
43. Phillips, M. C. 2014. Molecular mechanisms of cellular cholesterol efflux. J. Biol. Chem. 289:24020-24029.
44. Meyers, K. J., J. A. Mares, Z. Liu, C. K. Karki, B. Blodi, R. P. Igo, Jr., B. Truitt, S. K. Iyengar, A. E. Millen, M. Klein, et al. 2014. Genetic evidence for role of carotenoids in age-related macular degeneration in the carotenoids in age-related eye disease study (CAREDS). Invest. Ophthalmol. Vis. Sci. 55:587-599.
45. Rodrigueza, W. V., S. T. Thuahnai, R. E. Temel, S. Lund-Katz, M. C. Phillips, and D. L. Williams. 1999. Mechanism of scavenger receptor class B type I-mediated selective uptake of cholesteryl esters from high density lipoprotein to adrenal cells. J. Biol. Chem. 274:20344-20350.
46. Neculai, D., M. Schwake, M. Ravichandran, F. Zunke, R. F. Collins, J. Peters, M. Neculai, J. Plumb, P. Loppnau, J. C. Pizarro, et al. 2013. Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature. 504:172-176.
47. 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.
48. 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.
49. Reboul, E., A. Klein, F. Bietrix, B. Gleize, C. Malezet-Desmoulins, M. Schneider, A. Margotat, L. Lagrost, X. Collet, and P. Borel. 2006. Scavenger receptor class B type I (SR-BI) is involved in vitamin E transport across the enterocyte. J. Biol. Chem. 281:4739-4745.
50. Nieland, T. J., A. Chroni, M. L. Fitzgerald, Z. Maliga, V. I. Zannis, T. Kirchhausen, and M. Krieger. 2004. Cross-inhibition of SR-BIand ABCA1-mediated cholesterol transport by the small molecules BLT-4 and glyburide. J. Lipid Res. 45:1256-1265.
51. Yu, M., K. A. Romer, T. J. Nieland, S. Xu, V. Saenz-Vash, M. Penman, A. Yesilaltay, S. A. Carr, and M. Krieger. 2011. Exoplasmic cysteine Cys384 of the HDL receptor SR-BI is critical for its sensitivity to a small-molecule inhibitor and normal lipid transport activity. Proc. Natl. Acad. Sci. USA. 108:12243-12248.
52. 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.
53. Voolstra, O., C. Kiefer, M. Hoehne, R. Welsch, K. Vogt, and J. von Lintig. 2006. The Drosophila class B scavenger receptor NinaD-I is a cell surface receptor mediating carotenoid transport for visual chromophore synthesis. Biochemistry. 45:13429-13437.
54. Tsuchida, K., and T. Sakudoh. 2015. Recent progress in molecular genetic studies on the carotenoid transport system using cocooncolor mutants of the silkworm. Arch. Biochem. Biophys. 572:151-157.
55. Age-Related Eye Disease Study 2 Research Group. 2013. Lutein + zeaxanthin and omega-3 fatty acids for age-related macular degeneration: the Age-Related Eye Disease Study 2 (AREDS2) randomized clinical trial. JAMA. 309:2005-2015.
56. Maoka, T., A. Arai, M. Shimizu, and T. Matsuno. 1986. The first isolation of enantiomeric and meso-zeaxanthin in nature. Comp. Biochem. Physiol. B. 83:121-124.
57. Nolan, J. M., K. Meagher, S. Kashani, and S. Beatty. 2013. What is mesozeaxanthin, and where does it come from? Eye (Lond.). 27:899-905.
58. Thurnham, D. I., J. M. Nolan, A. N. Howard, and S. Beatty. 2015. Macular response to supplementation with differing xanthophyll formulations in subjects with and without age-related macular degeneration. Graefes Arch. Clin. Exp. Ophthalmol. 253:1231-1243.
59. Li, B., P. Vachali, J. M. Frederick, and P. S. Bernstein. 2011. Identification of StARD3 as a lutein-binding protein in the macula of the primate retina. Biochemistry. 50:2541-2549.
60. Wang, Y., S. L. Connor, W. Wang, E. J. Johnson, and W. E. Connor. 2007. The selective retention of lutein, meso-zeaxanthin and zeaxanthin in the retina of chicks fed a xanthophyll-free diet. Exp. Eye Res. 84:591-598.
61. 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.
62. Lindqvist, A., Y. G. He, and S. Andersson. 2005. Cell type-specific expression of beta-carotene 9', 10'-monooxygenase in human tissues. J. Histochem. Cytochem. 53:1403-1412.
63. Li, B., P. P. Vachali, A. Gorusupudi, Z. Shen, H. Sharifzadeh, B. M. Besch, K. Nelson, M. M. Horvath, J. M. Frederick, W. Baehr, et al. 2014. Inactivity of human β, β-carotene-9', 10'-dioxygenase (BCO2) underlies retinal accumulation of the human macular carotenoid pigment. Proc. Natl. Acad. Sci. USA. 111:10173-10178.
64. Babino, D., G. Palczewski, M. A. Widjaja-Adhi, P. D. Kiser, M. Golczak, and J. von Lintig. 2015. Characterization of the role of β-carotene 9, 10-dioxygenase in macular pigment metabolism. J. Biol. Chem. 290:24844-24857.
65. Palczewski, G., J. Amengual, C. L. Hoppel, and J. von Lintig. 2014. Evidence for compartmentalization of mammalian carotenoid metabolism. FASEB J. 28:4457-4469.