Genome-wide analysis of multi-ancestry cohorts identifies new loci influencing intraocular pressure and susceptibility to glaucoma

Nature Genetics

Volumn 46, Issue 10, 2014, Pages 1126-1130

  Hysi, Pirro G ^a   Cheng, Ching Yu ^b,c,d   Springelkamp, Henriët ^e   Macgregor, Stuart ^f   Cooke Bailey, Jessica N ^g,aw   Wojciechowski, Robert ^h,i   Vitart, Veronique ^j   Nag, Abhishek ^a   Hewitt, Alex W ^k   Höhn, René ^l   Venturini, Cristina ^a,m   Mirshahi, Alireza ^j   Ramdas, Wishal D ^l   Thorleifsson, Gudmar ^e   Vithana, Eranga ⁿ   Khor, Chiea Chuen ^b,c,d   Stefansson, Arni B ^c,o   Liao, Jiemin ^p   Haines, Jonathan L ^b,c,aw   Amin, Najaf ^g   Wang, Ya Xing ^e   Wild, Philipp S ^q   Ozel, Ayse B ^l   Li, Jun Z ^r   Fleck, Brian W ^r   Zeller, Tanja ^s   Staffieri, Sandra E ^t   Teo, Yik Ying ^k   Cuellar Partida, Gabriel ^c   Luo, Xiaoyan ^f   Allingham, R Rand ^u,aw   Richards, Julia E ^v,aw   Senft, Andrea ^e   Karssen, Lennart C ^w   Zheng, Yingfeng ^e   Bellenguez, Céline ^b,c,aw   Xu, Liang ^x,y,z   Iglesias, Adriana I ^q   Wilson, James F ^e   Kang, Jae Hee ^aa,aw   Van Leeuwen, Elisabeth M ^ab   Jonsson, Vesteinn ^e   Thorsteinsdottir, Unnur ^ac   Despriet, Dominiek D G ⁿ   Ennis, Sarah ^e   Moroi, Sayoko E ^ad,aw   Martin, Nicholas G ^r   Jansonius, Nomdo M ^f   Yazar, Seyhan ^ae   Tai, E Shyong ^af   Amouyel, Philippe ^c,d   Kirwan, James ^x,y,z,ag   Van Koolwijk, Leonieke M E ^ah   Hauser, Michael A ^e,aw   Jonasson, Fridbert ^v,ai   Leo, Paul ^aj   Loomis, Stephanie J ^ak,aw   Fogarty, Rhys ^al   Rivadeneira, Fernando ^e,am   Kearns, Lisa ^k   Lackner, Karl J ^an   De Jong, Paulus T V M ^ao,ap,aq,au   Simpson, Claire L ⁱ   Pennell, Craig E ^ar   Oostra, Ben A ^e   Uitterlinden, André G ^e,am   Saw, Seang Mei ^b,c,d   Lotery, Andrew J ^as   Bailey Wilson, Joan E ⁱ   Hofman, Albert ^e,am   Vingerling, Johannes R ^e   Maubaret, Cécilia ^x,at   Pfeiffer, Norbert ^a   Wolfs, Roger C W ^e   Lemij, Hans G ^a   Young, Terri L ^al   Pasquale, Louis R ^n,aw   Delcourt, Cécile ^b,c   Spector, Timothy D ^a   Klaver, Caroline C W ^e   Small, Kerrin S ^a   Burdon, Kathryn P ^al   Stefansson, Kari ⁿ   Wong, Tien Yin ^b,c,aw   Viswanathan, Ananth C ^av,aw   Mackey, David A ^k,af   Craig, Jamie E ^al,av   Wiggs, Janey L ^ak,av,aw   Van Duijn, Cornelia M ^e,av   Hammond, Christopher J ^a   Mitchell, Paul ^aw   Wang, Jie Jin ^aw   Rochtchina, Elena ^aw   Attia, John ^aw   Scott, Rodney ^aw   Holliday, Elizabeth G ^aw   Baird, Paul N ^aw   Xie, Jing ^aw   Inouye, Michael ^aw   Sim, Xueling ^aw   Brilliant, Murray H ^aw   Budenz, Donald L ^aw   Christen, William G ^aw   Fingert, John ^aw   Friedman, David S ^aw   Gaasterland, Douglas ^aw   Gaasterland, Terry ^aw   Kraft, Peter ^aw   Lee, Richard K ^aw   Lichter, Paul A ^aw   Liu, Yutao ^aw   Pericak Vance, Margaret A ^aw   Realini, Anthony ^aw   Schuman, Joel S ^aw   Scott, William K ^aw   Singh, Kuldev ^aw   Sit, Arthur J ^aw   Vollrath, Douglas ^aw   Weinreb, Robert N ^aw   Wollstein, Gadi ^aw   Zack, Donald J ^aw   Zhang, Kang ^aw   Donnelly, Peter ^aw   Langford, Cordelia ^aw   Hunt, Sarah E ^aw   Bramon, Elvira ^aw   Brown, Matthew A ^aw   Casas, Juan P ^aw   Corvin, Aiden ^aw   Dronov, Serge ^aw   Duncanson, Audrey ^aw   Gray, Emma ^aw   Hammond, Naomi ^aw   Mathew, Christopher G ^aw   Palmer, Colin N A ^aw   Plomin, Robert ^aw   Rautanen, Anna ^aw   Sawcer, Stephen J ^aw   Trembath, Richard C ^aw   Waller, Matthew ^aw   Weston, Paul ^aw   Spencer, Chris C A ^aw   Band, Gavin ^aw   Freeman, Colin ^aw   Hellenthal, Garrett ^aw   Giannoulatou, Eleni ^aw   Pirinen, Matti ^aw   Pearson, Richard ^aw   Strange, Amy ^aw   Su, Zhan ^aw   Vukcevic, Damjan ^aw   more..

^a KING'S COLLEGE LONDON   (United Kingdom)

^b SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

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

^h JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

ⁱ NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^j UNIVERSITY OF EDINBURGH   (United Kingdom)

^k UNIVERSITY OF MELBOURNE   (Australia)

^l UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^m UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁿ DECODE GENETICS   (Iceland)

^o GENOME INSTITUTE OF SINGAPORE   (Singapore)

^p University Eye Clinic   (Iceland)

^q CAPITAL MEDICAL UNIVERSITY   (China)

^r UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^s PRINCESS ALEXANDRA EYE PAVILION   (United Kingdom)

^t UNIVERSITY HEART CENTER HAMBURG   (Germany)

^u DUKE UNIVERSITY EYE CENTER   (United States)

^v DUKE UNIVERSITY MEDICAL CENTER   (United States)

^w UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^x INSERM   (France)

^y UNIV LILLE   (France)

^z INSTITUT PASTEUR DE LILLE   (France)

^aa UNIVERSITY OF EDINBURGH   (United Kingdom)

^ab CHANNING LABORATORY   (United States)

^ac LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^ad UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^ae UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^af UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^ag LILLE UNIVERSITY HOSPITAL   (France)

^ah PORTSMOUTH HOSPITALS NHS TRUST   (United Kingdom)

^ai UNIVERSITY OF ICELAND   (Iceland)

^aj UNIVERSITY OF QUEENSLAND   (Australia)

^ak MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^al FLINDERS UNIVERSITY   (Australia)

^am Netherlands Genomics Initiative   (Netherlands)

^an Pulmonary Department   (Germany)

^ao NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^ap LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^aq ACADEMIC MEDICAL CENTER   (Netherlands)

^ar UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^as UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^at UNIVERSITÉ DE BORDEAUX   (France)

^au ROTTERDAM EYE HOSPITAL   (Netherlands)

^av UNIVERSITY COLLEGE LONDON   (United Kingdom)

^aw NONE

more..

Author keywords

[No Author keywords available]

Indexed keywords

AGED; ARTICLE; CHROMOSOME 11P; CHROMOSOME 3Q; CHROMOSOME 9; COHORT ANALYSIS; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; GLAUCOMA; HUMAN; INTRAOCULAR PRESSURE; META ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; VERY ELDERLY;

EID: 84919382642     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3087     Document Type: Article

References (52)

1. Quigley, H.A. & Broman, A.T. The number of people with glaucoma worldwide in 2010 and 2020. Br. J. Ophthalmol. 90, 262-267 (2006).
2. Heijl, A., Leske, M.C., Bengtsson, B., Hyman, L. & Hussein, M. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch. Ophthalmol. 120, 1268-1279 (2002).
3. Collaborative Normal-Tension Glaucoma Study Group. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Collaborative Normal-Tension Glaucoma Study Group. Am. J. Ophthalmol. 126, 498-505 (1998).
4. Kass, M.A. et al. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch. Ophthalmol. 120, 701-713 (2002).
5. Wolfs, R.C. et al. Genetic risk of primary open-angle glaucoma. Population-based familial aggregation study. Arch. Ophthalmol. 116, 1640-1645 (1998).
6. Sanflippo, P.G., Hewitt, A.W., Hammond, C.J. & Mackey, D.A. The heritability of ocular traits. Surv. Ophthalmol. 55, 561-583 (2010).
7. Burdon, K.P. et al. Genome-wide association study identifes susceptibility loci for open angle glaucoma at TMCO1 and CDKN2B-AS1. Nat. Genet. 43, 574-578 (2011).
8. van Koolwijk, L.M. et al. Common genetic determinants of intraocular pressure and primary open-angle glaucoma. PLoS Genet. 8, e1002611 (2012).
9. Shah, S. et al. Relationship between corneal thickness and measured intraocular pressure in a general ophthalmology clinic. Ophthalmology 106, 2154-2160 (1999).
10. Devlin, B. & Roeder, K. Genomic control for association studies. Biometrics 55, 997-1004 (1999).
11. Higgins, J.P. & Thompson, S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 21, 1539-1558 (2002).
12. Dudbridge, F. & Gusnanto, A. Estimation of signifcance thresholds for genomewide association scans. Genet. Epidemiol. 32, 227-234 (2008).
13. Thorleifsson, G. et al. Common variants near CAV1 and CAV2 are associated with primary open-angle glaucoma. Nat. Genet. 42, 906-909 (2010).
14. Ozel, A.B. et al. Genome-wide association study and meta-analysis of intraocular pressure. Hum. Genet. 133, 41-57 (2014).
15. Do, R. et al. Common variants associated with plasma triglycerides and risk for coronary artery disease. Nat. Genet. 45, 1345-1352 (2013).
16. Grundberg, E. et al. Mapping cis-and trans-regulatory effects across multiple tissues in twins. Nat. Genet. 44, 1084-1089 (2012).
17. Moayyeri, A., Hammond, C.J., Hart, D.J. & Spector, T.D. The UK Adult Twin Registry (TwinsUK Resource). Twin Res. Hum. Genet. 16, 144-149 (2013).
18. Hofman, A. et al. The Rotterdam Study: 2012 objectives and design update. Eur. J. Epidemiol. 26, 657-686 (2011).
19. Lu, Y. et al. Genome-wide association analyses identify multiple loci associated with central corneal thickness and keratoconus. Nat. Genet. 45, 155-163 (2013).
20. Tonnu, P.A. et al. The infuence of central corneal thickness and age on intraocular pressure measured by pneumotonometry, non-contact tonometry, the Tono-Pen XL, and Goldmann applanation tonometry. Br. J. Ophthalmol. 89, 851-854 (2005).
21. Denis, M. et al. Expression, regulation, and activity of ABCA1 in human cell lines. Mol. Genet. Metab. 78, 265-274 (2003).
22. Yeghiazaryan, K. et al. An enhanced expression of ABC 1 transporter in circulating leukocytes as a potential molecular marker for the diagnostics of glaucoma. Amino Acids 28, 207-211 (2005).
23. Denomme, G.A. et al. Consortium for Blood Group Genes (CBGG): 2009 report. Immunohematology 26, 47-50 (2010).
24. Khan, M.I. et al. Association of ABO blood groups with glaucoma in the Pakistani population. Can. J. Ophthalmol. 44, 582-586 (2009).
25. Janssen, S.F. et al. Gene expression and functional annotation of the human ciliary body epithelia. PLoS ONE 7, e44973 (2012).
26. Charlesworth, J. et al. The path to open-angle glaucoma gene discovery: endophenotypic status of intraocular pressure, cup-to-disc ratio, and central corneal thickness. Invest. Ophthalmol. Vis. Sci. 51, 3509-3514 (2010).
27. Purcell, S.M. et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 460, 748-752 (2009).
28. Carbonaro, F., Andrew, T., Mackey, D.A., Spector, T.D. & Hammond, C.J. Comparison of three methods of intraocular pressure measurement and their relation to central corneal thickness. Eye (Lond.) 24, 1165-1170 (2010).
29. Mitchell, P., Smith, W., Attebo, K. & Wang, J.J. Prevalence of age-related maculopathy in Australia. The Blue Mountains Eye Study. Ophthalmology 102, 1450-1460 (1995).
30. Foran, S., Wang, J.J. & Mitchell, P. Causes of visual impairment in two older population cross-sections: the Blue Mountains Eye Study. Ophthalmic Epidemiol. 10, 215-225 (2003).
31. Aulchenko, Y.S. et al. Linkage disequilibrium in young genetically isolated Dutch population. Eur. J. Hum. Genet. 12, 527-534 (2004).
32. Pardo, L.M., MacKay, I., Oostra, B., van Duijn, C.M. & Aulchenko, Y.S. The effect of genetic drift in a young genetically isolated population. Ann. Hum. Genet. 69, 288-295 (2005).
33. Leibowitz, H.M. et al. The Framingham Eye Study monograph: an ophthalmological and epidemiological study of cataract, glaucoma, diabetic retinopathy, macular degeneration, and visual acuity in a general population of 2631 adults, 1973-1975. Surv. Ophthalmol. 24, 335-610 (1980).
34. Vitart, V. et al. New loci associated with central cornea thickness include COL5A1, AKAP13 and AVGR8. Hum. Mol. Genet. 19, 4304-4311 (2010).
35. Evans, S., Newnham, J., MacDonald, W. & Hall, C. Characterisation of the possible effect on birthweight following frequent prenatal ultrasound examinations. Early Hum. Dev. 45, 203-214 (1996).
36. Newnham, J.P., Evans, S.F., Michael, C.A., Stanley, F.J. & Landau, L.I. Effects of frequent ultrasound during pregnancy: a randomised controlled trial. Lancet 342, 887-891 (1993).
37. Williams, L.A., Evans, S.F. & Newnham, J.P. Prospective cohort study of factors infuencing the relative weights of the placenta and the newborn infant. Br. Med. J. 314, 1864-1868 (1997).
38. Hofman, A. et al. The Rotterdam Study: 2014 objectives and design update. Eur. J. Epidemiol. 28, 889-926 (2013).
39. Mackey, D.A. et al. Twins eye study in Tasmania (TEST): rationale and methodology to recruit and examine twins. Twin Res. Hum. Genet. 12, 441-454 (2009).
40. Spector, T.D. & Williams, F.M. The UK Adult Twin Registry (TwinsUK). Twin Res. Hum. Genet. 9, 899-906 (2006).
41. Wang, Y.X., Xu, L., Yang, H. & Jonas, J.B. Prevalence of glaucoma in North China: the Beijing Eye Study. Am. J. Ophthalmol. 150, 917-924 (2010).
42. Lavanya, R. et al. Methodology of the Singapore Indian Chinese Cohort (SICC) eye study: quantifying ethnic variations in the epidemiology of eye diseases in Asians. Ophthalmic Epidemiol. 16, 325-336 (2009).
43. Foong, A.W. et al. Rationale and methodology for a population-based study of eye diseases in Malay people: the Singapore Malay eye study (SiMES). Ophthalmic Epidemiol. 14, 25-35 (2007).
44. 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. 39, 906-913 (2007).
45. Howie, B.N., Donnelly, P. & Marchini, J. A fexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 5, e1000529 (2009).
46. Li, Y., Willer, C.J., Ding, J., Scheet, P. & Abecasis, G.R. MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet. Epidemiol. 34, 816-834 (2010).
47. van der Valk, R. et al. Intraocular pressure-lowering effects of all commonly used glaucoma drugs: a meta-analysis of randomized clinical trials. Ophthalmology 112, 1177-1185 (2005).
48. Stephens, M. & Balding, D.J. Bayesian statistical methods for genetic association studies. Nat. Rev. Genet. 10, 681-690 (2009).
49. Higgins, J.P., Thompson, S.G., Deeks, J.J. & Altman, D.G. Measuring inconsistency in meta-analyses. Br. Med. J. 327, 557-560 (2003).
50. Liu, J.Z. et al. A versatile gene-based test for genome-wide association studies. Am. J. Hum. Genet. 87, 139-145 (2010).
51. Nagelkerke, N.J.D. A note on a general defnition of the coeffcient of determination. Biometrika 78, 691-692 (1991).
52. Rozen, S. & Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386 (2000).