© 2011 Nature America, Inc. All rights reserved. © 2011 Nature America, Inc. All rights reserved.
NATURE GENETICS VOLUME 43 | NUMBER 12 | DECEMBER 2011 1219
Gastric cancer is a heterogeneous disease with multiple
environmental etiologies and alternative pathways of
carcinogenesis
1,2
. Beyond mutations in TP53, alterations in
other genes or pathways account for only small subsets of
the disease. We performed exome sequencing of 22 gastric
cancer samples and identified previously unreported mutated
genes and pathway alterations; in particular, we found genes
involved in chromatin modification to be commonly mutated.
A downstream validation study confirmed frequent inactivating
mutations or protein deficiency of ARID1A, which encodes a
member of the SWI-SNF chromatin remodeling family, in 83%
of gastric cancers with microsatellite instability (MSI), 73%
of those with Epstein-Barr virus (EBV) infection and 11% of
those that were not infected with EBV and microsatellite stable
(MSS). The mutation spectrum for ARID1A differs between
molecular subtypes of gastric cancer, and mutation prevalence
is negatively associated with mutations in TP53. Clinically,
ARID1A alterations were associated with better prognosis
in a stage-independent manner. These results reveal the
genomic landscape, and highlight the importance of chromatin
remodeling, in the molecular taxonomy of gastric cancer.
Recent studies using next-generation sequencing (NGS) have
revealed an extensive repertoire of potential cancer-driving genes
in several cancer types
3–17
. To further explore the genetic basis
of gastric cancer, we performed whole-exome capture using the
Agilent SureSelect Human All Exon kit followed by NGS on the
Illumina Genome Analyzer II× or HiSeq 2000 platforms to iden-
tify somatic mutations in 22 matched pairs of gastric cancer and
normal tissue (Supplementary Table 1), with a mean depth of 116×
and 91.4% of bases covered to at least 10× (Supplementary Table 2).
Somatic mutations were predicted using algorithms described in
the Supplementary Note, and an extensive subset was confirmed
by Sequenom MassARRAY genotyping (Supplementary Table 3),
giving a positive prediction rate of 96.8% (95% confidence interval
(CI), 95.2–98.4%) for somatic single-nucleotide variation (SNV)
and 97.9% (95% CI, 95.8–99.9%) for somatic insertion or deletion
(indel) alterations.
Overall, 7,036 somatic mutations were detected in the 22 gastric
cancer samples, of which 4,653 occurred in coding regions or essen-
tial splice sites (2,513 missense, 137 nonsense, 5 stop codon loss,
90 splice site, 855 indel and 1,053 synonymous mutations) (Table 1 and
Supplementary Table 4). Consistent with the known consequences of
mismatch repair deficiency, the gastric cancer samples with MSI had an
average of 31.61 somatic mutations (including both SNVs and indels)
per megabase of DNA, whereas the MSS gastric cancer samples had an
average of 3.29, a difference of approximately tenfold. Likewise, MSI
gastric cancer samples had an average of 620 protein-altering somatic
mutations, which was tenfold higher than the the number found in
MSS gastric cancer samples (mean of 62). Although there was no sig-
nificant difference in the nonsynonymous-to-synonymous (NS/S)
ratio between the MSI and the MSS gastric cancers, we found a signifi-
cantly higher NS/S ratio in EBV-infected gastric cancer samples (4.55 ±
0.97 compared to 2.76 ± 0.72 in non-EBV–infected gastric cancer
samples, P < 0.012) and in poorly differentiated gastric cancers (3.52 ±
0.94 compared to 2.56 ± 0.78 in well- and moderately differentiated
gastric cancers, P < 0.014), suggestive of a higher positive selection
pressure for driver mutations in these subgroups
18,19
. Of note, the NS/S
ratio for the EBV-infected gastric cancer samples (range 3.64–5.56) is
among the highest for solid organ cancers (range 0.97–3.5) reported to
date
3,8–10,12,17
. C-to-T transitions were the most common mutation
(51%) across all gastric cancers, with 68% involving CG dinucleotides.
The MSI gastric cancers also had a distinctly high rate of T-to-C transi-
tions (30%) (Supplementary Table 5). The observed mutation incidence
for MSS gastric cancers (3.29 per megabase) is higher than our previous
results from sequencing the kinome of most other cancers (0.74–1.85 per
megabase for renal, colorectal and ovarian cancers) but lower than in
lung cancers (4.21 per megabase)
20
. The observed mutation spectrum
Exome sequencing identifies frequent mutation of
ARID1A in molecular subtypes of gastric cancer
Kai Wang
1,7
, Junsuo Kan
2,7
, Siu Tsan Yuen
2
, Stephanie T Shi
3
, Kent Man Chu
4
, Simon Law
4
, Tsun Leung Chan
2
,
Zhengyan Kan
1
, Annie S Y Chan
2
, Wai Yin Tsui
2
, Siu Po Lee
2
, Siu Lun Ho
2
, Anthony K W Chan
2
,
Grace H W Cheng
2
, Peter C Roberts
5
, Paul A Rejto
1
, Neil W Gibson
1,6
, David J Pocalyko
1
, Mao Mao
1
,
Jiangchun Xu
1
& Suet Yi Leung
2
1
Oncology Research Unit, Pfizer Worldwide Research and Development, La Jolla, California, USA.
2
Department of Pathology, The University of Hong Kong, Queen
Mary Hospital, Pokfulam, Hong Kong.
3
External Research Solutions, Pfizer Worldwide Research and Development, La Jolla, California, USA.
4
Department of Surgery,
The University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong.
5
Research Embedded Business Technology, Pfizer Worldwide Research and Development,
La Jolla, California, USA.
6
Present address: Regulus Therapeutics, San Diego, California, USA.
7
These authors contributed equally to this work. Correspondence
should be addressed to S.Y.L. (suetyi@hku.hk) or J.X. (jiangchun.xu@pfizer.com).
Received 18 May; accepted 23 September; published online 30 October 2011; doi:10.1038/ng.982
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