Apolipoprotein E genotype is associated with macular pigment optical density

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 5, 2010, Pages 2636-2643

  Loane, Edward ^a,b   McKay, Gareth J ^c   Nolan, John M ^a   Beatty, Stephen ^a,d  

^a Ireland   (Ireland)

^b ROYAL VICTORIA EYE AND EAR HOSPITAL   (Ireland)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d Whitfield Clinic   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

XANTHOPHYLL; ZEAXANTHIN; APOLIPOPROTEIN E; VISUAL PIGMENT;

ADULT; AGE; AGED; APOE GENE; ARTICLE; BODY MASS; CIGARETTE SMOKING; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIETARY INTAKE; FOOD FREQUENCY QUESTIONNAIRE; GENE; GENOTYPE; HUMAN; NORMAL HUMAN; OPTICAL DENSITY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; SEX; CHEMISTRY; DENSITOMETRY; DIET; FEEDING BEHAVIOR; FEMALE; GENETICS; LIGHT RELATED PHENOMENA; MALE; MIDDLE AGED; NUTRITION; RETINA; SMOKING;

ADULT; AGED; APOLIPOPROTEINS E; BODY MASS INDEX; CROSS-SECTIONAL STUDIES; DENSITOMETRY; DIET; FEMALE; FOOD HABITS; GENOTYPE; HUMANS; LUTEIN; MALE; MIDDLE AGED; NUTRITION SURVEYS; OPTICAL PROCESSES; RETINA; RETINAL PIGMENTS; SMOKING; XANTHOPHYLLS; YOUNG ADULT;

EID: 77952472259     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4397     Document Type: Article

References (83)

1. Bressler NM. Age-related macular degeneration is the leading cause of blindness. JAMA. 2004;291(15):1900-1901.
2. Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA. 2003;290(15):2057-2060.
3. Klein R, Wang Q, Klein BEK, Moss SE, Meuer SM. The relationship of age-related maculopathy, cataract, and glaucoma to visual acuity. Invest Ophthalmol Vis Sci. 1995;36(1):182-191.
4. van Leeuwen R, Klaver CC, Vingerling JR, Hofman A, de Jong PT. Epidemiology of age-related maculopathy: a review. Eur J Epidemiol. 2003;18(9):845-854.
5. Tomany SC, Wang HJ, van Leeuwen R, et al. Risk factors for incident age-related macular degeneration: pooled findings from 3 continents. Ophthalmology. 2004;111(7):1280-1287.
6. Nolan JM, Stack J, O'Donovan O, Loane E, Beatty S. Risk factors for age-related maculopathy are associated with a relative lack of macular pigment. Exp Eye Res. 2007;84(1):61-74.
7. Bone RA, Landrum JT, Hime GW, Cains A, Zamor J. Stereochemistry of the human macular carotenoids. Invest Ophthalmol Vis Sci. 1993;34(6):2033-2040.
8. Johnson EJ, Neuringer M, Russell RM, Schalch W, Snodderly DM. 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. 2005;46(2):692-702.
9. Bialostosky K, Wright JD, Kennedy-Stephenson J, McDowell M, Johnson CL. Dietary intake of macronutrients, micronutrients, and other dietary constituents: United States 1988-94. Vital Health Stat. 2002;(245):1-158.
10. Bone RA, Landrum JT, Fernandez L, Tarsis SL. Analysis of the macular pigment by HPLC: retinal distribution and age study. Invest Ophthalmol Vis Sci. 1988;29(6):843-849.
11. Snodderly DM, Handelman GJ, Adler AJ. Distribution of individual macular pigment carotenoids in central retina of macaque and squirrel monkeys. Invest Ophthalmol Vis Sci. 1991;32(2):268-279.
12. Snodderly DM. Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. Am J Clin Nutr. 1995;62(6):S1448-S1461.
13. Liew SHM, Gilbert C, Spector TD, et al. Heritability of macular pigment: a twin study. Invest Ophthalmol Vis Sci. 2005;46(12):4430-4436.
14. Baird PN, Guida E, Chu DT, Vu HTV, Guymer RH. The ε2 and ε4 alleles of the apolipoprotein gene are associated with age-related macular degeneration. Invest Ophthalmol Vis Sci. 2004;45(5):1311-1315.
15. Klaver CC, Kliffen M, van Duijn CM, et al. Genetic association of apolipoprotein E with age-related macular degeneration. Am J Hum Genet. 1998;63(1):200-206.
16. Simonelli F, Margaglione M, Testa F, et al. Apolipoprotein E polymorphisms in age-related macular degeneration in an Italian population. Ophthalmic Res. 2001;33(6):325-328.
17. Souied EH, Benlian P, Amouyel P, et al. The epsilon4 allele of the apolipoprotein E gene as a potential protective factor for exudative age-related macular degeneration. Am J Ophthalmol. 1998; 125(3):353-359.
18. Zareparsi S, Reddick AC, Branham KEH, et al. Association of apolipoprotein E alleles with susceptibility to age-related macular degeneration in a large cohort from a single center. Invest Ophthalmol Vis Sci. 2004;45(5):1306-1310.
19. Utermann G, Langenbeck U, Beisiegel U, Weber W. Genetics of the apolipoprotein E system in man. Am J Hum Genet. 1980;32(3):339-347.
20. Bojanowski CM, Shen D, Chew EY, et al. An apolipoprotein E variant may protect against age-related macular degeneration through cytokine regulation. Environ Mol Mutagen. 2006;47(8):594-602.
21. Fritsche LG, Freitag-Wolf S, Bettecken T, et al. Age-related macular degeneration and functional promoter and coding variants of the apolipoprotein E gene. Hum Mutat. 2009;30(7):1048-1053.
22. Boyles JK, Zoellner CD, Anderson LJ, et al. A role for apolipoprotein E, apolipoprotein A-I, and low density lipoprotein receptors in cholesterol transport during regeneration and remyelination of the rat sciatic nerve. J Clin Invest. 1989;83(3):1015-1031.
23. Erdman JW Jr, Bierer TL, Gugger ET. Absorption and transport of carotenoids. Ann N Y Acad Sci. 1993;691:76-85.
24. Goulinet S, Chapman MJ. Plasma LDL and HDL subspecies are heterogenous in particle content of tocopherols oxygenated and hydrocarbon carotenoids: relevance to oxidative resistance and atherogenesis. Arterioscler Thromb Vasc Biol. 1997;17(4):786-796.
25. Yeum KJ, Russell RM. Carotenoid bioavailability and bioconversion. Annu Rev Nutr. 2002;22:483-504.
26. Leon AS, Togashi K, Rankinen T, et al. Association of apolipoprotein E polymorphism with blood lipids and maximal oxygen uptake in the sedentary state and after exercise training in the HERITAGE family study. Metabolism. 2004;53(1):108-116.
27. Willett WC. Future directions in the development of food-frequency questionnaires. Am J Clin Nutr. 1994;59(1):S171-S174.
28. Bodner CH, Soutar A, New SA, et al. Validation of a food frequency questionnaire for use in a Scottish population: correlation of antioxidant vitamin intakes with biochemical measures. J Hum Nutr Dietetics. 1998;11(5):373-380.
29. Masson LF, McNeill G, Tomany JO, et al. Statistical approaches for assessing the relative validity of a food-frequency questionnaire: use of correlation coefficients and the kappa statistic. Public Health Nutr. 2003;6(3):313-321.
30. O'Connell ED, Nolan JM, Stack J, et al. Diet and risk factors for age-related maculopathy. Am J Clin Nutr. 2008;87(3):712-722.
31. Nolan JM, Stack J, Mellerio J, Godhinio M, O'Donovan O, Beatty S. Monthly consistency of macular pigment optical density and serum concentrations of lutein and zeaxanthin. Curr Eye Res. 2006; 31(2):199-213.
32. Holland B, Welch AA, Unwin ID, Buss DH, Paul AA, Southgate DAT. McCance and Widdowson's The Composition of Foods. Fifth revised and extended edition. London: Food Standards Agency; 1991.
33. O'Neill ME, Carroll Y, Corridan B, et al. A European carotenoid database to assess carotenoid intakes and its use in a five-country comparative study. Br J Nutr. 2001;85(4):499-507.
34. United States Department of Agriculture. USDA-NCC Carotenoid Database for U.S. Foods-1998. http://www.nal.usda.gov/fnic/foodcomp/Data/car98/car98.html. Accessed January 2, 2010.
35. Foods Standards Agency. McCance and Widdowson's The Composition of Foods. Sixth summary edition. Cambridge: Royal Society of Chemistry; 2002.
36. Rand WM, Windham CT, Wyse BW, Young VR. Compiling Data for Food Composition Databases. Tokyo: United Nations University Press; 1991.
37. Bone RA, Landrum JT, Cains A. Optical density spectra of the macular pigment in vivo and in vitro. Vis Res. 1992;32(1):105-110.
38. Wooten BR, Hammond BR, Land RI, Snodderly DM. A practical method for measuring macular pigment optical density. Invest Ophthalmol Vis Sci. 1999;40(11):2481-2489.
39. Nolan JM, Stringham JM, Beatty S, Snodderly DM. Spatial profile of macular pigment and its relationship to foveal architecture. Invest Ophthalmol Vis Sci. 2008;49(5):2134-2142.
40. Loane E, Stack J, Beatty S, Nolan JM. Measurement of macular pigment optical density using two different heterochromatic flicker photometers. Curr Eye Res. 2007;32(6):555-564.
41. Mellerio J, Ahmadi-Lari S, van Kuijk FJGM, Pauleikhoff D, Bird AC, Marshall J. A portable instrument for measuring macular pigment with central fixation. Curr Eye Res. 2002;25(1):37-47.
42. Beatty S, Murray IJ, Henson DB, Carden D, Koh HH, Boulton ME. Macular pigment and risk for age-related macular degeneration in subjects from a Northern European population. Invest Ophthalmol Vis Sci. 2001;42(2):439-446.
43. Snodderly DM, Mares JA, Wooten BR, Oxton L, Gruber M, Ficek T. Macular pigment measurement by heterochromatic flicker photometry in older subjects: the carotenoids and age-related eye disease study. Invest Ophthalmol Vis Sci. 2004;45(2):531-538.
44. Ciulla TA, Curran-Celantano J, Cooper DA, et al. Macular pigment optical density in a midwestern sample. Ophthalmology. 2001; 108(4):730-737.
45. Hammond BR, Caruso-Avery M. Macular pigment optical density in a southwestern sample. Invest Ophthalmol Vis Sci. 2000;41(6):1492-1497.
46. Bennet AM, Di AE, Ye Z, et al. Association of apolipoprotein E genotypes with lipid levels and coronary risk. JAMA. 2007; 298(11):1300-1311.
47. Laws SM, Hone E, Gandy S, Martins RN. Expanding the association between the APOE gene and the risk of Alzheimer's disease: possible roles for APOE promoter polymorphisms and alterations in APOE transcription. J Neurochem. 2003;84(6):1215-1236.
48. Thakkinstian A, Bowe S, McEvoy M, Smith W, Attia J. Association between apolipoprotein E polymorphisms and age-related macular degeneration: a HuGE review and meta-analysis. Am J Epidemiol. 2006;164(9):813-822.
49. Schmidt S, Klaver C, Saunders A, et al. A pooled case-control study of the apolipoprotein E (APOE gene in age-related maculopathy. Ophthalmic Genet. 2002;23(4):209-223.
50. Friedman DA, Lukiw WJ, Hill JM. Apolipoprotein E epsilon4 offers protection against age-related macular degeneration. Med Hypotheses. 2007;68(5):1047-1055.
51. Loane E, Kelliher C, Beatty S, Nolan JM. The rationale and evidence base for a protective role of macular pigment in age-related maculopathy. Br J Ophthalmol. 2008;92(9):1163-1168.
52. Krinsky NI, Deneke SM. Interaction of oxygen and oxy-radicals with carotenoids. J Natl Cancer Inst. 1982;69(1):205-210.
53. Lim BP, Nagao A, Terao J, Tanaka K, Suzuki T, Takama K. Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. Biochim Biophys Acta. 1992; 1126(2):178-184.
54. Snodderly DM, Auran JD, Delori FC. The macular pigment, II: spatial distribution in primate retinas. Invest Ophthalmol Vis Sci. 1984;25(6):674-685.
55. Ham WT Jr, Mueller HA, Sliney DH. Retinal sensitivity to damage from short wavelength light. Nature. 1976;260(5547):153-155.
56. Organisciak DT, Darrow RA, Barsalou L, Darrow RM, Lininger LA. Light-induced damage in the retina: differential effects of dimethylthiourea on photoreceptor survival, apoptosis and DNA oxidation. Photochem Photobiol. 1999;70(2):261-268.
57. Khachik F, Bernstein PS, Garland DL. Identification of lutein and zeaxanthin oxidation products in human and monkey retinas. Invest Ophthalmol Vis Sci. 1997;38(9):1802-1811.
58. Kennedy CJ, Rakoczy PE, Constable IJ. Lipofuscin of the retinal pigment epithelium: a review. Eye. 1995;9:763-771.
59. Rozanowska M, Jarvis-Evans J, Korytowski W, Boulton ME, Burke JM, Sarna T. Blue light-induced reactivity of retinal age pigment: in vitro generation of oxygen-reactive species. J Biol Chem. 1995 270(32):18825-18830.
60. Boulton M, Dontsov A, Jarvisevans J, Ostrovsky M, Svistunenko D. Lipofuscin is a photoinducible free-radical generator. J Photochem Photobiol B-Biol. 1993;19(3):201-204.
61. Wing GL, Blanchard GC, Weiter JJ. Topography and age relationship of lipofuscin concentration in retinal-pigment epithelium. Invest Ophthalmol Vis Sci. 1978;17(7):601-607.
62. Weiter JJ, Delori FC, Wing GL, Fitch KA. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Invest Ophthalmol Vis Sci. 1986;27(2):145-152.
63. Reboul E, Abou L, Mikail C, et al. 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.
64. Clevidence BA, Bieri JG. Association of carotenoids with human plasma lipoproteins. Methods Enzymol. 1993;214:33-46.
65. Connor WE, Duell PB, Kean R, Wang Y. The prime role of HDL to transport lutein into the retina: evidence from HDL-deficient WHAM chicks having a mutant ABCA1 transporter. Invest Ophthalmol Vis Sci. 2007;48(9):4226-4231.
66. Wang W, Connor SL, Johnson EJ, Klein ML, Hughes S, Connor WE. Effect of dietary lutein and zeaxanthin on plasma carotenoids and their transport in lipoproteins in age-related macular degeneration. Am J Clin Nutr. 2007;85(3):762-769.
67. Bhosale P, Larson AJ, Frederick JM, Southwick K, Thulin CD, Bernstein PS. Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1 as a zeaxanthin-binding protein in the macula of the human eye. J Biol Chem. 2004;279(47):49447-49454.
68. Bernstein PS, Balashov NA, Tsong ED, Rando RR. Retinal tubulin binds macular carotenoids. Invest Ophthalmol Vis Sci. 1997;38(1):167-175.
69. Bhosale P, Li B, Sharifzadeh M, et al. Purification and partial characterization of a lutein-binding protein from human retina. Biochemistry. 2009;48(22):4798-4807.
70. Mahley RW, Innerarity TL, Rall SC Jr, Weisgraber KH. Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res. 1984;25(12):1277-1294.
71. Gregg RE, Zech LA, Schaefer EJ, Stark D, Wilson D, Brewer HB Jr. Abnormal in vivo metabolism of apolipoprotein E4 in humans. J Clin Invest. 1986;78(3):815-821.
72. Anderson DH, Ozaki S, Nealon M, et al. Local cellular sources of apolipoprotein E in the human retina and retinal pigmented epithelium: implications for the process of drusen formation. Am J Ophthalmol. 2001;131(6):767-781.
73. Shanmugaratnam J, Berg E, Kimerer L, et al. Retinal Muller glia secrete apolipoproteins E and J which are efficiently assembled into lipoprotein particles. Brain Res Mol Brain Res. 1997;50(1-2):113-120.
74. Dentchev T, Milam AH, Lee VM, Trojanowski JQ, Dunaief JL. Amyloid-beta is found in drusen from some age-related macular degeneration retinas, but not in drusen from normal retinas. Mol Vis. 2003;9:184-190.
75. Dithmar S, Curcio CA, Le NA, Brown S, Grossniklaus HE. Ultrastructural changes in Bruch's membrane of apolipoprotein Edeficient mice. Invest Ophthalmol Vis Sci. 2000;41(8):2035-2042.
76. Conley YP, Thalamuthu A, Jakobsdottir J, et al. Candidate gene analysis suggests a role for fatty acid biosynthesis and regulation of the complement system in the etiology of age-related maculopathy. Hum Mol Genet. 2005;14(14):1991-2002.
77. Gotoh N, Kuroiwa S, Kikuchi T, et al. Apolipoprotein E polymorphisms in Japanese patients with polypoidal choroidal vasculopathy and exudative age-related macular degeneration. Am J Ophthalmol. 2004;138(4):567-573.
78. Pang CP, Baum L, Chan WM, Lau TC, Poon PM, Lam DS. The apolipoprotein E epsilon4 allele is unlikely to be a major risk factor of age-related macular degeneration in Chinese. Ophthalmologica. 2000;214(4):289-291.
79. Schmidt S, Haines JL, Postel EA, et al. Joint effects of smoking history and APOE genotypes in age-related macular degeneration. Mol Vis. 2005;11:941-949.
80. Schultz DW, Klein ML, Humpert A, et al. Lack of an association of apolipoprotein E gene polymorphisms with familial age-related macular degeneration. Arch Ophthalmol. 2003;121(5):679-683.
81. Wong TY, Shankar A, Klein R, et al. Apolipoprotein E gene and early age-related maculopathy: the Atherosclerosis Risk in Communities Study. Ophthalmology. 2006;113(2):255-259.
82. Utheim OA, Ritland JS, Utheim TP, et al. Apolipoprotein E genotype and risk for development of cataract and age-related macular degeneration. Acta Ophthalmol. 2008;86(4):401-403.
83. Stewart JE, Skinner ER, Best PV. Receptor binding of an apolipoprotein E-rich subfraction of high density lipoprotein to rat and human brain membranes. Int J Biochem Cell Biol. 1998;30(3):407-415.