Genome-wide association identifies SKIV2L and MYRIP as protective factors for age-related macular degeneration

Genes and Immunity

Volumn 11, Issue 8, 2010, Pages 609-621

  Kopplin, L J ^a   Igo, R P ^b   Wang Jr , Y ^b   Sivakumaran, T A ^b   Hagstrom, S A ^a,c   Peachey, N S ^a,c,d   Francis, P J ^e   Klein, M L ^e   Sangiovanni, J P ^f   Chew, E Y ^f   Pauer, G J T ^c   Sturgill, G M ^d   Joshi, T ^b   Tian, L ^b   Xi, Q ^b   Henning, A K ^g   Lee, K E ^h   Klein, R ^h   Klein, B E K ^h   Iyengar, S K ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^f NATIONAL EYE INSTITUTE   (United States)

^g EMMES CORPORATION   (United States)

^h UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

association testing; macular degeneration; melanosome trafficking

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H;

ADULT; AGED; ALLELE; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; GENE LOCUS; GENE REPLICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MELANOSOME; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AGED; AGED, 80 AND OVER; ALLELES; COMPLEMENT FACTOR H; DNA HELICASES; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; MACULAR DEGENERATION; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 78649691414     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2010.39     Document Type: Article

References (85)

1. Klein R, Klein BE, Knudtson MD, Meuer SM, Swift M, Gangnon RE. Fifteen-year cumulative incidence of age-related macular degeneration: the Beaver Dam Eye Study. Ophthalmology 2007; 114: 253-262.
2. Klein R, Klein BE, Tomany SC, Meuer SM, Huang GH. Ten-year incidence and progression of age-related maculopathy: the Beaver Dam eye study. Ophthalmology 2002; 109: 1767-1779.
3. Mitchell P, Wang JJ, Foran S, Smith W. Five-year incidence of age-related maculopathy lesions: the Blue Mountains Eye Study. Ophthalmology 2002; 109: 1092-1097. (Pubitemid 34546916)
4. Wang JJ, Rochtchina E, Lee AJ, Chia EM, Smith W, Cumming RG et al. Ten-year incidence and progression of age-related maculopathy: the blue Mountains Eye Study. Ophthalmology 2007; 114: 92-98. (Pubitemid 46014292)
5. Peeters A, Magliano DJ, Stevens J, Duncan BB, Klein R, Wong TY. Changes in abdominal obesity and age-related macular degeneration: the atherosclerosis risk in communities study. Arch Ophthalmol 2008; 126: 1554-1560.
6. 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.
7. Edwards AO, Ritter III R, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 2005; 308: 421-424.
8. Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 2005; 308: 419-421.
9. Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS, Haynes C et al. Complement factor H polymorphism in age-related macular degeneration. Science 2005; 308: 385-389.
10. Li M, Atmaca-Sonmez P, Othman M, Branham KE, Khanna R, Wade MS 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.
11. Gold B, Merriam JE, Zernant J, Hancox LS, Taiber AJ, Gehrs K et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat Genet 2006; 38: 458-462.
12. McKay GJ, Silvestri G, Patterson CC, Hogg RE, Chakravarthy U, Hughes AE. Further assessment of the complement component 2 and factor B region associated with age-related macular degeneration. Invest Ophthalmol Vis Sci 2009; 50: 533-539.
13. Spencer KL, Hauser MA, Olson LM, Schmidt S, Scott WK, Gallins P et al. Protective effect of complement factor B and complement component 2 variants in age-related macular degeneration. Hum Mol Genet 2007; 16: 1986-1992. (Pubitemid 47354881)
14. Yates JR, Sepp T, Matharu BK, Khan JC, Thurlby DA, Shahid H et al. Complement C3 variant and the risk of age-related macular degeneration. N Engl J Med 2007; 357: 553-561.
15. Dewan A, Liu M, Hartman S, Zhang SS, Liu DT, Zhao C et al. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science 2006; 314: 989-992.
16. 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.
17. Kanda A, Chen W, Othman M, Branham KE, Brooks M, Khanna R et al. A variant of mitochondrial protein LOC387715/ARMS2, not HTRA1, is strongly associated with age-related macular degeneration. Proc Natl Acad Sci USA 2007; 104: 16227-16232.
18. Rivera A, Fisher SA, Fritsche LG, Keilhauer CN, Lichtner P, Meitinger T 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.
19. Yang Z, Camp NJ, Sun H, Tong Z, Gibbs D, Cameron DJ et al. A variant of the HTRA1 gene increases susceptibility to age-related macular degeneration. Science 2006; 314: 992-993.
20. Fritsche LG, Loenhardt T, Janssen A, Fisher SA, Rivera A, Keilhauer CN et al. Age-related macular degeneration is associated with an unstable ARMS2 (LOC387715) mRNA. Nat Genet 2008; 40: 892-896.
21. SanGioVanni JP, Arking DE, Iyengar SK, Elashoff M, Clemons TE, Reed GF et al. Mitochondrial DNA variants of respiratory complex I that uniquely characterize haplogroup T2 are associated with increased risk of age-related macular degeneration. PLoS ONE 2009; 4: e5508.
22. Canter JA, Olson LM, Spencer K, Schnetz-Boutaud N, Anderson B, Hauser MA et al. Mitochondrial DNA polymorphism A4917G is independently associated with age-related macular degeneration. PLoS ONE 2008; 3: e2091.
23. Mullins RF, Russell SR, Anderson DH, Hageman GS. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J 2000; 14: 835-846.
24. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI 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 USA 2005; 102: 7227-7232.
25. Zipfel PF, Hallstrom T, Hammerschmidt S, Skerka C. The complement fitness factor H: role in human diseases and for immune escape of pathogens, like pneumococci. Vaccine 2008; 26(Suppl 8): I67-I74.
26. Coffey PJ, Gias C, McDermott CJ, Lundh P, Pickering MC, Sethi C et al. Complement factor H deficiency in aged mice causes retinal abnormalities and visual dysfunction. Proc Natl Acad Sci USA 2007; 104: 16651-16656.
27. Dupuis J, Langenberg C, Prokopenko I, Saxena R, Soranzo N, Jackson AU et al. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat Genet 2010; 42: 105-116.
28. Kathiresan S, Willer CJ, Peloso GM, Demissie S, Musunuru K, Schadt EE et al. Common variants at 30 loci contribute to polygenic dyslipidemia. Nat Genet 2009; 41: 56-65.
29. Newton-Cheh C, Johnson T, Gateva V, Tobin MD, Bochud M, Coin L et al. Genome-wide association study identifies eight loci associated with blood pressure. Nat Genet 2009; 41: 666-676.
30. Cupples LA, Arruda HT, Benjamin EJ, D'Agostino Sr RB, Demissie S, DeStefano AL et al. The Framingham Heart Study 100K SNP genome-wide association study resource: overview of 17 phenotype working group reports. BMC Med Genet 2007; 8(Suppl 1): S1.
31. Maller J, George S, Purcell S, Fagerness J, Altshuler D, Daly MJ 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.
32. El-Amraoui A, Schonn JS, Kussel-Andermann P, Blanchard S, Desnos C, Henry JP et al. MyRIP, a novel Rab effector, enables myosin VIIa recruitment to retinal melanosomes. EMBO Rep 2002; 3: 463-470.
33. Klomp AE, Teofilo K, Legacki E, Williams DS. Analysis of the linkage of MYRIP and MYO7A to melanosomes by RAB27A in retinal pigment epithelial cells. Cell Motil Cytoskeleton 2007; 64: 474-487.
34. Augustin I, Rosenmund C, Sudhof TC, Brose N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 1999; 400: 457-461.
35. Augustin I, Korte S, Rickmann M, Kretzschmar HA, Sudhof TC, Herms JW et al. The cerebellum-specific Munc13 isoform Munc13-3 regulates cerebellar synaptic transmission and motor learning in mice. J Neurosci 2001; 21: 10-17.
36. Iyengar SK, Song D, Klein BE, Klein R, Schick JH, Humphrey J et al. Dissection of genome-wide-scan data in extended families reveals a major locus and oligogenic susceptibility for age-related macular degeneration. Am J Hum Genet 2004; 74: 20-39.
37. Schraermeyer U, Heimann K. Current understanding on the role of retinal pigment epithelium and its pigmentation. Pigment Cell Res 1999; 12: 219-236.
38. Bergmann M, Schutt F, Holz FG, Kopitz J. Inhibition of the ATP-driven proton pump in RPE lysosomes by the major lipofuscin fluorophore A2-E may contribute to the patho-genesis of age-related macular degeneration. FASEB J 2004; 18: 562-564.
39. Holz FG, Schutt F, Kopitz J, Eldred GE, Kruse FE, Volcker HE et al. Inhibition of lysosomal degradative functions in RPE cells by a retinoid component of lipofuscin. Invest Ophthalmol Vis Sci 1999; 40: 737-743.
40. Guo Y, Yao G, Lei B, Tan J. Monte Carlo model for studying the effects of melanin concentrations on retina light absorption. J Opt Soc Am A Opt Image Sci Vis 2008; 25: 304-311.
41. El-Amraoui A, Sahly I, Picaud S, Sahel J, Abitbol M, Petit C. Human Usher 1B/mouse shaker-1: the retinal phenotype discrepancy explained by the presence/absence of myosin VIIA in the photoreceptor cells. Hum Mol Genet 1996; 5: 1171-1178.
42. Weil D, Levy G, Sahly I, Levi-Acobas F, Blanchard S, El-Amraoui A et al. Human myosin VIIA responsible for the Usher 1B syndrome: a predicted membrane-associated motor protein expressed in developing sensory epithelia. Proc Natl Acad Sci USA 1996; 93: 3232-3237.
43. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J et al. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 1995; 374: 60-61.
44. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 1995; 92: 9815-9819.
45. Lopes VS, Ramalho JS, Owen DM, Karl MO, Strauss O, Futter CE et al. The ternary Rab27a-Myrip-Myosin VIIa complex regulates melanosome motility in the retinal pigment epithelium. Traffic 2007; 8: 486-499.
46. Kuroda TS, Fukuda M. Identification and biochemical analysis of Slac2-c/MyRIP as a Rab27A-, myosin Va/VIIa-, and actin-binding protein. Methods Enzymol 2005; 403: 431-444.
47. Ramalho JS, Lopes VS, Tarafder AK, Seabra MC, Hume AN. Myrip uses distinct domains in the cellular activation of myosin VA and myosin VIIA in melanosome transport. Pigment Cell Melanoma Res 2009; 22: 461-473.
48. Gibbs D, Kitamoto J, Williams DS. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc Natl Acad Sci USA 2003; 100: 6481-6486.
49. Schonthaler HB, Lampert JM, von Lintig J, Schwarz H, Geisler R, Neuhauss SC. A mutation in the silver gene leads to defects in melanosome biogenesis and alterations in the visual system in the zebrafish mutant fading vision. Dev Biol 2005; 284: 421-436.
50. Schraermeyer U, Peters S, Thumann G, Kociok N, Heimann K. Melanin granules of retinal pigment epithelium are connected with the lysosomal degradation pathway. Exp Eye Res 1999; 68: 237-245.
51. Warburton S, Davis WE, Southwick K, Xin H, Woolley AT, Burton GF et al. Proteomic and phototoxic characterization of melanolipofuscin: correlation to disease and model for its origin. Mol Vis 2007; 13: 318-329.
52. Lee SG, Lee I, Park SH, Kang C, Song K. Identification and characterization of a human cDNA homologous to yeast SKI2. Genomics 1995; 25: 660-666.
53. Schmid M, Jensen TH. The exosome: a multipurpose RNA-decay machine. Trends Biochem Sci 2008; 33: 501-510.
54. Bernstein KA, Granneman S, Lee AV, Manickam S, Baserga SJ. Comprehensive mutational analysis of yeast DEXD/H box RNA helicases involved in large ribosomal subunit biogenesis. Mol Cell Biol 2006; 26: 1195-1208. (Pubitemid 43202549)
55. Yang Z, Qu X, Yu CY. Features of the two gene pairs RD-SKI2W and DOM3Z-RP1 located between complement component genes factor B and C4 at the MHC class III region. Front Biosci 2001; 6: D927-D935.
56. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ et al. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 2001; 107: 451-464.
57. Wang AL, Lukas TJ, Yuan M, Du N, Tso MO, Neufeld AH. Autophagy and exosomes in the aged retinal pigment epithelium: possible releVance to drusen formation and age-related macular degeneration. PLoS ONE 2009; 4: e4160.
58. Kondo N, Honda S, Kuno SI, Negi A. Role of RDBP and SKIV2 L variants in the major histocompatibility complex class III region in polypoidal choroidal vasculopathy etiology. Ophthalmology 2009; 116: 1502-1509.
59. Fernando MM, Stevens CR, Sabeti PC, Walsh EC, McWhinnie AJ, Shah A et al. Identification of two independent risk factors for lupus within the MHC in United Kingdom families. PLoS Genet 2007; 3: e192.
60. Edwards AO, Fridley BL, James KM, Sharma AK, Cunningham JM, Tosakulwong N. Evaluation of clustering and genotype distribution for replication in genome-wide association studies: the age-related eye disease study. PLoS One 2008; 3: e3813.
61. Zhang H, Morrison MA, Dewan A, Adams S, Andreoli M, Huynh N et al. The NEI/NCBI dbGAP database: genotypes and haplotypes that may specifically predispose to risk of neovascular age-related macular degeneration. BMC Med Genet 2008; 9: 51.
62. Klein R, Knudtson MD, Klein BE, Wong TY, Cotch MF, Liu K et al. Inflammation, complement factor h, and age-related macular degeneration: the multi-ethnic Study of Atherosclerosis. Ophthalmology 2008; 115: 1742-1749.
63. Tedeschi-Blok N, Buckley J, Varma R, Triche TJ, Hinton DR. Population-based study of early age-related macular degeneration: role of the complement factor H Y402H polymorphism in bilateral but not unilateral disease. Ophthalmology 2007; 114: 99-103.
64. Grassi MA, Fingert JH, Scheetz TE, Roos BR, Ritch R, West SK et al. Ethnic variation in AMD-associated complement factor H polymorphism p.Tyr402His. Hum Mutat 2006; 27: 921-925.
65. Chu J, Zhou CC, Lu N, Zhang X, Dong FT. Genetic variants in three genes and smoking show strong associations with susceptibility to exudative age-related macular degeneration in a Chinese population. Chin Med J (Engl) 2008; 121: 2525-2533.
66. Xu Y, Guan N, Xu J, Yang X, Ma K, Zhou H et al. Association of CFH, LOC387715, and HTRA1 polymorphisms with exudative age-related macular degeneration in a northern Chinese population. Mol Vis 2008; 14: 1373-1381.
67. 0UTR in age-related macular degeneration. Hum Genet 2010; 127: 595-602.
68. Orlin A, Hadley D, Brown G, Brucker A, Ho A, Regillo C et al. The relationship between the A69S variant with the indel (372-815delins54) in the ARMS2 gene, and its association with age-related macular degeneration. Invest Ophthalmol Vi s S c i 2009; 50: E-Abstract 1601.
69. Yang Z, Tong Z, Chen Y, Zeng J, Lu F, Sun X et al. Genetic and functional dissection of HTRA1 and LOC387715 in age-related macular degeneration. PLoS Genet 2010; 6: e1000836.
70. Fei H, Grygoruk A, Brooks ES, Chen A, Krantz DE. Trafficking of vesicular neurotransmitter transporters. Traffic 2008; 9: 1425-1436.
71. Newell-Litwa K, Seong E, Burmeister M, Faundez V. Neuronal and non-neuronal functions of the AP-3 sorting machinery. J Cell Sci 2007; 120(Part 4): 531-541.
72. Mailman MD, Feolo M, Jin Y, Kimura M, Tryka K, Bagoutdinov R et al. The NCBI dbGaP database of genotypes and pheno-types. Nat Genet 2007; 39: 1181-1186.
73. Age Related Eye Disease Study Group. Risk factors associated with age-related macular degeneration. A case-control study in the age-related eye disease study: age-related eye disease study report number 3. Ophthalmology 2000: 107; 2224-2232.
74. Ferris FL, Davis MD, Clemons TE, Lee LY, Chew EY, Lindblad AS et al. A simplified severity scale for age-related macular degeneration: AREDS report no. 18. Arch Ophthalmol 2005; 123: 1570-1574.
75. Klein R, Klein BE, Jensen SC, Meuer SM. The five-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology 1997; 104: 7-21. (Pubitemid 27081937)
76. Klein R, Klein BE, Linton KL. Prevalence of age-related maculopathy. The Beaver Dam Eye Study. Ophthalmology 1992; 99: 933-943.
77. S.A.G.E. Statistical Analysis for Genetic Epidemiology 2007. http://genepi.cwru.edu.
78. Marchini J, Howie B, Myers S, McVean G, Donnelly P. A new multipoint method for genome-wide association studies by imputation of genotypes. Nat Genet 2007; 39: 906-913.
79. Devlin B, Roeder K. Genomic control for association studies. Biometrics 1999; 55: 997-1004.
80. Purcell S. PLINK 2008. http://pngu.mgh.harvard.edu/pur-cell/plink.
81. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575.
82. Li Y, Abecasis GR. MaCH 1.0: rapid haplotype reconstruction and missing genotype inference. Am J Hum Genet 2006; S79: 2290.
83. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001; 68: 978-989.
84. Stephens M, Scheet P. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 2005; 76: 449-462.
85. Schaid DJ. Evaluating associations of haplotypes with traits. Genet Epidemiol 2004; 27: 348-364.