Association of variants in the LIPC and ABCA1 genes with intermediate and large drusen and advanced age-related macular degeneration

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 7, 2011, Pages 4663-4670

  Yu, Yi ^a   Reynolds, Robyn ^a   Fagerness, Jesen ^b,c   Rosner, Bernard ^d   Daly, Mark J ^b,c   Seddon, Johanna M ^a,e  

^a TUFTS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d CHANNING LABORATORY   (United States)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; APOLIPOPROTEIN E; CHOLESTEROL ESTER TRANSFER PROTEIN; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H; COMPLEMENT FACTOR I; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIVER TRIACYLGLYCEROL LIPASE; SERINE PROTEINASE; ABC TRANSPORTER; LIPH PROTEIN, HUMAN; TRIACYLGLYCEROL LIPASE;

AGED; ALLELE; ARTICLE; ATP BINDING CASSETTE SUBFAMILY A MEMBER 1 GENE; CONTROLLED STUDY; DISEASE SEVERITY; DRUSEN; FEMALE; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC RISK; GENOTYPE; GENOTYPING TECHNIQUE; HEPATIC LIPASE GENE; HEREDITY; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; SINGLE NUCLEOTIDE POLYMORPHISM; GENETIC PREDISPOSITION; GENETIC VARIABILITY; GENETICS; HOSPITALIZATION; OPTIC DISK ANOMALY; PATHOLOGY; PHENOTYPE; RETINA MACULA DEGENERATION;

AGED; AGED, 80 AND OVER; ATP-BINDING CASSETTE TRANSPORTERS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GENOTYPE; HUMANS; LIPASE; MACULAR DEGENERATION; MALE; OPTIC DISK DRUSEN; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SEVERITY OF ILLNESS INDEX;

EID: 80052197495     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-7070     Document Type: Article

References (69)

1. Seddon JM, Sobrin L. Epidemiology of age-related macular degeneration. In: Albert D, Miller J, Azar D, Blodi B, eds. Albert & Jakobiec's Principles and Practice of Ophthalmology. Philadelphia: WB Saunders; 2007:413-422.
2. Friedman DS, O'Colmain BJ, Munoz B, et al. Prevalence of agerelated macular degeneration in the United States. Arch Ophthalmol. 2004;122:564-572.
3. de Jong PT. Age-related macular degeneration. N Engl J Med. 2006;355:1474-1485.
4. Zarbin MA. Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol. 2004;122:598-614.
5. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, Mullins RF. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res. 2001;20:705-732.
6. Fariss RN, Apte SS, Olsen BR, Iwata K, Milam AH. Tissue inhibitor of metalloproteinases-3 is a component of Bruch's membrane of the eye. Am J Pathol. 1997;150:323-328.
7. Hageman GS, Mullins RF, Russell SR, Johnson LV, Anderson DH. Vitronectin is a constituent of ocular drusen and the vitronectin gene is expressed in human retinal pigmented epithelial cells. FASEB J. 1999;13:477-484.
8. Luibl V, Isas JM, Kayed R, Glabe CG, Langen R, Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J Clin Invest. 2006;116:378-385.
9. Johnson LV, Leitner WP, Staples MK, Anderson DH. Complement activation and inflammatory processes in drusen formation and age related macular degeneration. Exp Eye Res. 2001;73:887-896.
10. Li CM, Clark ME, Rudolf M, Curcio CA. Distribution and composition of esterified and unesterified cholesterol in extra-macular drusen. Exp Eye Res. 2007;85:192-201.
11. Wang L, Clark ME, Crossman DK, et al. Abundant lipid and protein components of drusen. PLoS One. 2010;5:e10329.
12. Curcio CA, Johnson M, Huang JD, Rudolf M. Apolipoprotein B-containing lipoproteins in retinal aging and age-related macular degeneration. J Lipid Res. 2010;51:451-467.
13. Seddon JM, Cote J, Page WF, Aggen SH, Neale MC. The US twin study of age-related macular degeneration: relative roles of genetic and environmental influences. Arch Ophthalmol. 2005;123:321-327.
14. Seddon JM, Willett WC, Speizer FE, Hankinson SE. A prospective study of cigarette smoking and age-related macular degeneration in women. JAMA. 1996;276:1141-1146.
15. Seddon JM, Cote J, Davis N, Rosner B. Progression of age-related macular degeneration: association with body mass index, waist circumference, and waist-hip ratio. Arch Ophthalmol. 2003;121: 785-792.
16. Tomany SC, Wang JJ, Van Leeuwen R, et al. Risk factors for incident age-related macular degeneration: pooled findings from 3 continents. Ophthalmology. 2004;111:1280-1287.
17. Clemons TE, Milton RC, Klein R, Seddon JM, Ferris FL 3rd. Risk factors for the incidence of advanced age-related macular degeneration in the Age-Related Eye Disease Study (AREDS). AREDS report no. 19. Ophthalmology 2005;112:533-539.
18. Seddon JM, George S, Rosner B, Klein ML. CFH gene variant, Y402H, and smoking, body mass index, environmental associations with advanced age-related macular degeneration. Hum Hered. 2006;61:157-165.
19. Seddon JM, George S, Rosner B. Cigarette smoking, fish consumption, omega-3 fatty acid intake, and associations with age-related macular degeneration: the US Twin Study of Age-Related Macular Degeneration. Arch Ophthalmol. 2006;124:995-1001.
20. Seddon JM, Francis PJ, George S, Schultz DW, Rosner B, Klein ML. Association of CFH Y402H and LOC387715 A69S with progression of age-related macular degeneration. JAMA. 2007;297:1793-1800.
21. Haines JL, Hauser MA, Schmidt S, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308:419-421.
22. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005;308: 385-389.
23. Hageman GS, Anderson DH, Johnson LV, et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A. 2005;102:7227-7232.
24. Maller J, George S, Purcell S, et al. Common variation in three genes, including a noncoding variant in CFH, strongly influences risk of age-related macular degeneration. Nat Genet. 2006;38: 1055-1059.
25. Li M, Atmaca-Sonmez P, Othman M, et al. CFH haplotypes without the Y402H coding variant show strong association with susceptibility to age-related macular degeneration. Nat Genet. 2006;38: 1049-1054.
26. Edwards AO, Ritter R 3rd, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science. 2005;308:421-424.
27. Gold B, Merriam JE, Zernant J, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with agerelated macular degeneration. Nat Genet. 2006;38:458-462.
28. Maller JB, Fagerness JA, Reynolds RC, Neale BM, Daly MJ, Seddon JM. Variation in complement factor 3 is associated with risk of age-related macular degeneration. Nat Genet. 2007;39:1200-1201.
29. Yates JR, Sepp T, Matharu BK, et al. Complement C3 variant and the risk of age-related macular degeneration. N Engl J Med. 2007;357:553-561.
30. Fagerness JA, Maller JB, Neale BM, Reynolds RC, Daly MJ, Seddon JM. Variation near complement factor I is associated with risk of advanced AMD. Eur J Hum Genet. 2009;17:100-104.
31. Rivera A, Fisher SA, Fritsche LG, et al. Hypothetical LOC387715 is a second major susceptibility gene for age-related macular degeneration, contributing independently of complement factor H to disease risk. Hum Mol Genet. 2005;14:3227-3236.
32. Yang Z, Camp NJ, Sun H, et al. A variant of the HTRA1 gene increases susceptibility to age-related macular degeneration. Science. 2006;314:992-993.
33. Seddon JM, Reynolds R, Rosner B. Peripheral retinal drusen and reticular pigment: association with CFHY402H and CFHrs1410996 genotypes in family and twin studies. Invest Ophthalmol Vis Sci. 2009;50:586-591.
34. Andreoli MT, Morrison MA, Kim BJ, et al. Comprehensive analysis of complement factor H and LOC387715/ARMS2/HTRA1 variants with respect to phenotype in advanced age-related macular degeneration. Am J Ophthalmol. 2009;148:869-874.
35. Magnusson KP, Duan S, Sigurdsson H, et al. CFH Y402H confers similar risk of soft drusen and both forms of advanced AMD. PLoS Med. 2006;3:e5.
36. Grassi MA, Folk JC, Scheetz TE, Taylor CM, Sheffield VC, Stone EM. Complement factor H polymorphism p. Tyr402His and cuticular drusen. Arch Ophthalmol. 2007;125:93-97.
37. Hasham SN, Pillarisetti S. Vascular lipases, inflammation and atherosclerosis. Clin Chim Acta. 2006;372:179-183.
38. Kathiresan S, Willer CJ, Peloso GM, et al. Common variants at 30 loci contribute to polygenic dyslipidemia. Nat Genet. 2009;41:56-65.
39. Neale BM, Fagerness J, Reynolds R, et al. Genome-wide association study of advanced age-related macular degeneration identifies a role of the hepatic lipase gene (LIPC). Proc Natl Acad Sci U S A. 2010;107:7395-7400.
40. Chen W, Stambolian D, Edwards AO, et al. Genetic variants near TIMP3 and high-density lipoprotein-associated loci influence susceptibility to age-related macular degeneration. Proc Natl Acad Sci U S A. 2010;107:7401-7406.
41. 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;125:353-359.
42. Baird PN, Richardson AJ, Robman LD, et al. Apolipoprotein (APOE) gene is associated with progression of age-related macular degeneration (AMD). Hum Mutat. 2006;27:337-342.
43. Losonczy G, Fekete A, Voko Z, et al. Analysis of complement factor H Y402H, LOC387715, HTRA1 polymorphisms and ApoE alleles with susceptibility to age-related macular degeneration in Hungarian patients. Acta Ophthalmol. 2011;89:255-262.
44. 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;30:1048-1053.
45. Seddon JM, Sharma S, Adelman RA. Evaluation of the clinical age-related maculopathy staging system. Ophthalmology. 2006;113:260-266.
46. The Age-Related Eye Disease Study (AREDS): design implications. AREDS report no. 1. Control Clin Trials 1999;20:573-600.
47. Dewan A, Liu M, Hartman S, et al. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science. 2006;314:989-992.
48. Jakobsdottir J, Conley YP, Weeks DE, Mah TS, Ferrell RE, Gorin MB. Susceptibility genes for age-related maculopathy on chromosome 10q26. Am J Hum Genet. 2005;77:389-407.
49. Purcell S, Neale B, Todd-Brown K, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559-575.
50. Seddon JM, Reynolds R, Rosner B. Associations of smoking, body mass index, dietary lutein, and the LIPC gene variant rs10468017 with advanced age-related macular degeneration. Mol Vis. 2010;16:2412-2424.
51. Reynolds R, Rosner B, Seddon JM. Serum lipid biomarkers and hepatic lipase gene associations with age-related macular degeneration. Ophthalmology. 2010;117:1989-1995.
52. Rufibach LE, Duncan SA, Battle M, Deeb SS. Transcriptional regulation of the human hepatic lipase (LIPC) gene promoter. J Lipid Res. 2006;47:1463-1477.
53. Grarup N, Andreasen CH, Andersen MK, et al. The-250G>A promoter variant in hepatic lipase associates with elevated fasting serum high-density lipoprotein cholesterol modulated by interaction with physical activity in a study of 16,156 Danish subjects. J Clin Endocrinol Metab. 2008;93:2294-2299.
54. Tserentsoodol N, Gordiyenko NV, Pascual I, Lee JW, Fliesler SJ, Rodriguez IR. Intraretinal lipid transport is dependent on high density lipoprotein-like particles and class B scavenger receptors. Mol Vis. 2006;12:1319-1333.
55. Duncan KG, Hosseini K, Bailey KR, et al. Expression of reverse cholesterol transport proteins ATP-binding cassette A1 (ABCA1) and scavenger receptor BI (SR-BI) in the retina and retinal pigment epithelium. Br J Ophthalmol. 2009;93:1116-1120.
56. Nong Z, Gonzalez-Navarro H, Amar M, et al. Hepatic lipase expression in macrophages contributes to atherosclerosis in apoE-deficient and LCAT-transgenic mice. J Clin Invest. 2003;112:367-378.
57. Gonzalez-Navarro H, Nong Z, Freeman L, Bensadoun A, Peterson K, Santamarina-Fojo S. Identification of mouse and human macrophages as a site of synthesis of hepatic lipase. J Lipid Res. 2002;43:671-675.
58. Schmitz G, Kaminski WE, Porsch-Ozcurumez M, et al. ATP-binding cassette transporter A1 (ABCA1) in macrophages: a dual function in inflammation and lipid metabolism? Pathobiology. 1999;67: 236-240.
59. Oram JF, Lawn RM, Garvin MR, Wade DP. ABCA1 is the cAMPinducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J Biol Chem. 2000;275:34508-34511.
60. Lucas AD, Greaves DR. Atherosclerosis: role of chemokines and macrophages. Expert Rev Mol Med. 2001;3:1-18.
61. Tang C, Liu Y, Kessler PS, Vaughan AM, Oram JF. The macrophage cholesterol exporter ABCA1 functions as an anti-inflammatory receptor. J Biol Chem. 2009;284:32336-32343.
62. Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Biol. 2010;30:139-143.
63. Curcio CA, Rudolf M, Wang L. Histochemistry and lipid profiling combine for insights into aging and age-related maculopathy. Methods Mol Biol. 2009;580:267-281.
64. Curcio CA, Johnson M, Huang JD, Rudolf M. Aging, age-related macular degeneration, and the response-to-retention of apolipoprotein B-containing lipoproteins. Prog Retin Eye Res. 2009;28: 393-422.
65. Cherepanoff S, McMenamin PG, Gillies MC, Kettle E, Sarks SH. Bruch's membrane and choroidal macrophages in early and advanced age-related macular degeneration. Br J Ophthalmol. 2010;94:918-925.
66. Killingsworth MC, Sarks JP, Sarks SH. Macrophages related to Bruch's membrane in age-related macular degeneration. Eye (Lond). 1990;4(Pt 4):613-621.
67. Boon CJ, Klevering BJ, Hoyng CB, et al. Basal laminar drusen caused by compound heterozygous variants in the CFH gene. Am J Hum Genet. 2008;82:516-523.
68. Munch IC, Ek J, Kessel L, et al. Small, hard macular drusen and peripheral drusen: associations with AMD genotypes in the Inter99 Eye Study. Invest Ophthalmol Vis Sci. 2010;51:2317-2321.
69. Seddon JM, Reynolds R, Maller J, Fagerness JA, Daly MJ, Rosner B. Prediction model for prevalence and incidence of advanced age-related macular degeneration based on genetic, demographic, and environmental variables. Invest Ophthalmol Vis Sci. 2009;50:2044-2053.