NATURE GENETICS VOLUME 45 | NUMBER 11 | NOVEMBER 2013 1371
Through whole-genome sequencing of 2,230 Icelanders, we
detected a rare nonsynonymous SNP (minor allele frequency =
0.55%) in the C3 gene encoding a p.Lys155Gln substitution in
complement factor 3, which, following imputation into a set of
Icelandic cases with age-related macular degeneration (AMD)
and controls, associated with disease (odds ratio (OR) = 3.45;
P = 1.1 × 10
-7
). This signal is independent of the previously
reported common SNPs in C3 encoding p.Pro314Leu and
p.Arg102Gly that associate with AMD. The association of
p.Lys155Gln was replicated in AMD case-control samples
of European ancestry with OR = 4.22 and P = 1.6 × 10
-10
,
resulting in OR = 3.65 and P = 8.8 × 10
-16
for all studies
combined. In vitro studies have suggested that the p.Lys155Gln
substitution reduces C3b binding to complement factor H,
potentially creating resistance to inhibition by this factor.
This resistance to inhibition in turn is predicted to result
in enhanced complement activation.
AMD is the major cause of blindness in the elderly in the Western
part of the world
1
. Previous genome-wide association studies (GWAS)
of AMD have yielded common variants at 12 loci (Supplementary
Table 1 and GWAS catalog; see URLs
2
). Two of these encode com-
ponents of the complement pathway, CFH on chromosome 1 and
C2-CFB on chromosome 6, and have been reported to harbor more
than one independent common association signal
3
. Recently, a very
rare nonsynonymous mutation in CFH, encoding p.Arg1210Cys, was
identified and reported to confer high risk of AMD
4
.
The aim of the current study was to search for new rare and low-
frequency variants, identified through whole-genome sequencing,
that associate with AMD. Sequence variants, including SNPs and
indels, were identified through whole-genome sequencing of 2,230
Icelanders to an average sequencing depth of 10×. Using imputa-
tion assisted by long-range phased haplotypes, we determined the
genotype probabilities of all 34.2 million sequence variants identified
for 95,085 Icelanders genotyped with Illumina SNP chips (Online
Methods). We then tested for association of the identified variants
using 1,143 Icelanders diagnosed with AMD (neovascular disease,
geographic atrophy or soft drusen) and 51,435 Icelandic controls
with genotype information from whole-genome sequencing (Online
Methods). Apart from some of the previously reported loci, no new
loci had associations that reached the threshold of genome-wide sig-
nificance (P < 1.5 × 10
-9
) (Supplementary Fig. 1).
As an additional rare variant has been described in the CFH
gene that confers high risk of AMD
4
, we next decided to exam-
ine associations within the loci previously reported to associate
with AMD by performing conditional analysis (Online Methods
and Supplementary Table 2). Of the 12 established AMD loci, the
strongest signal at 6 reached the significance level of P = 1.0 × 10
-5
in our data, which we set as the threshold for applying conditional
analysis. These six loci were APOE, ARMS2-HTRA1, C2-CFB, CFH,
A rare nonsynonymous sequence variant in C3 is associated
with high risk of age-related macular degeneration
Hannes Helgason
1,2,17
, Patrick Sulem
1,17
, Maheswara R Duvvari
3
, Hongrong Luo
4–7
, Gudmar Thorleifsson
1
,
Hreinn Stefansson
1
, Ingileif Jonsdottir
1,8,9
, Gisli Masson
1
, Daniel F Gudbjartsson
1,2
, G Bragi Walters
1
,
Olafur Th Magnusson
1
, Augustine Kong
1,2
, Thorunn Rafnar
1
, Lambertus A Kiemeney
10,11
,
Frederieke E Schoenmaker-Koller
3
, Ling Zhao
4,5
, Camiel J F Boon
3
, Yaojun Song
4,5
, Sascha Fauser
12
,
Michelle Pei
4,5
, Tina Ristau
12
, Shirrina Patel
4,5
, Sandra Liakopoulos
12
, Johannes P H van de Ven
3
,
Carel B Hoyng
3
, Henry Ferreyra
4,5
, Yaou Duan
4–7
, Paul S Bernstein
13
, Asbjorg Geirsdottir
14
,
Gudleif Helgadottir
14
, Einar Stefansson
8,14
, Anneke I den Hollander
3,15
, Kang Zhang
4–7,16
,
Fridbert Jonasson
9,14
, Haraldur Sigurdsson
14
, Unnur Thorsteinsdottir
1,9
& Kari Stefansson
1,9
1
deCODE Genetics/Amgen, Reykjavik, Iceland.
2
School of Engineering and Natural Sciences, University of Iceland, Reykjavik, Iceland.
3
Department of Ophthalmology,
Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands.
4
Department of Ophthalmology, University of California, San Diego, La Jolla, California,
USA.
5
Institute for Genomic Medicine, University of California, San Diego, La Jolla, California, USA.
6
Department of Ophthalmology, West China Hospital, Sichuan
University, Chengdu, China.
7
Molecular Medicine Research Center, West China Hospital, Sichuan University, Chengdu, China.
8
Department of Immunology, National
University Hospital, Reykjavik, Iceland.
9
Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
10
Department for Health Evidence, Radboud University Medical
Center, Nijmegen, The Netherlands.
11
Department of Urology, Radboud University Medical Center, Nijmegen, The Netherlands.
12
Department of Ophthalmology,
University Hospital of Cologne, Cologne, Germany.
13
Moran Eye Center, University of Utah, Salt Lake City, Utah, USA.
14
Department of Ophthalmology, National
University Hospital, Reykjavik, Iceland.
15
Department of Human Genetics, Nijmegen Center for Molecular Life Sciences and Institute of Genetic and Metabolic
Diseases, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands.
16
Veterans Affairs Healthcare System, San Diego, California, USA.
17
These
authors contributed equally to this work. Correspondence should be addressed to P.S. (patrick.sulem@decode.is) or K.S. (kstefans@decode.is).
Received 24 January; accepted 31 July; published online 15 September 2013; doi:10.1038/ng.2740
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