804 VOLUME 45 | NUMBER 7 | JULY 2013 NATURE GENETICS
LETTERS
To identify genetic risk factors underlying non-Hodgkin
lymphomas (NHLs) from the B cell lineage, we conducted
a genome-wide association study (GWAS) of 253 Chinese
individuals with B cell NHL (cases) and 1,438 controls and
further validation in 1,175 cases and 5,492 controls.
We identified a new susceptibility locus, rs6773854, located
between BCL6 (encoding B cell lymphoma protein 6) and
LPP (encoding lipoma preferred partner) on oncogene-rich
chromosome 3q27 that was significantly associated with
increased risk of B cell NHL (meta-analysis P = 3.36 × 10
−13
,
per-allele odds ratio (OR) = 1.44) and with diffuse large B cell
lymphoma (DLBCL) in particular (meta-analysis P = 1.14 × 10
−11
,
OR = 1.47). We found no evidence of association of rs6773854
with non–B cell NHLs (T cell and natural killer (NK) lineages)
(P = 0.17, OR = 1.12) and observed significant heterogeneity
between B cell and non–B cell subtypes (P
het
= 0.01,
I
2
= 84%). Our results provide insight that germline
variation in the intergenic region between BCL6 and LPP
has a role in risk of B cell lymphomagenesis.
NHLs (MIM 605027), a complex group of malignant tumors aris-
ing from lymphoid tissue, are characterized by the clonal expansion
of tumorigenic immune cells in various stages of differentiation
1
.
NHLs from B cell lineages are more common, with DLBCL being
the most common and aggressive histological subtype worldwide
1,2
.
In support of a genetic basis for the disease, NHLs were observed
to exhibit familial aggregation, and up to tenfold increased risk
has been reported for the first-degree relatives of probands with
DLBCL
3
. Although genetic risk factors have been hypothesized to
be specific to each histological subtype of NHL, epidemiological
studies suggest that some of these risk factors may be shared by
different subtypes
4
.
Several genetic association studies have been performed in search
of common risk variants for NHL
5–8
; however, these studies were
predominantly conducted in individuals of European ancestry, and
investigation in Asians has been lacking. Besides robust associations
reported between HLA (human leukocyte antigen) variants and risk
of follicular lymphoma
5–7
, no other genome-wide significant locus has
been identified for the other NHL subtypes. Hence, to gain insights
into genetic susceptibility factors for B cell NHLs in Asians, we con-
ducted a GWAS of 274 Chinese individuals with B cell NHL and 1,500
controls recruited in Singapore. After applying stringent quality filters
(Online Methods), there were 253 B cell NHLs (including 51 follicular
lymphomas, 54 marginal zone lymphomas and 148 DLBCLs), 1,438
controls (Supplementary Table 1a) and 550,946 autosomal SNPs
available for association analysis.
Genome-wide association study of B cell non-Hodgkin
lymphoma identifies 3q27 as a susceptibility locus in the
Chinese population
Dennis E K Tan
1,22
, Jia Nee Foo
1,22
, Jin-Xin Bei
1,2,22
, Jiang Chang
3,4,22
, Roujun Peng
2
, Xiaohui Zheng
2
,
Lixuan Wei
3,4
, Ying Huang
3,4
, Wei Yen Lim
5
, Juan Li
6
, Qian Cui
2
, Soo Hong Chew
7
, Richard P Ebstein
8
,
Ponnudurai Kuperan
9
, Soon Thye Lim
10
, Miriam Tao
10
, Suat Hoon Tan
11
, Alvin Wong
12
, Gee Chuan Wong
13
,
Soo Yong Tan
14
, Siok Bian Ng
15
, Yi-Xin Zeng
2,16
, Chiea Chuen Khor
1,5,17–19
, Dongxin Lin
3,4,23
,
Adeline L H Seow
5,23
, Wei-Hua Jia
2,23
& Jianjun Liu
1,5,20,21,23
1
Human Genetics, Genome Institute of Singapore, Agency for Science, Technology and Research (A*STAR), Singapore.
2
State Key Laboratory of Oncology in South
China, Sun Yat-sen University Cancer Center, Guangzhou, China.
3
State Key Laboratory of Molecular Oncology, Cancer Institute and Hospital, Chinese Academy of
Medical Science and Peking Union Medical College, Beijing, China.
4
Department of Etiology and Carcinogenesis, Cancer Institute and Hospital, Chinese Academy of
Medical Science and Peking Union Medical College, Beijing, China.
5
Saw Swee Hock School of Public Health, National University Health System, National University
of Singapore, Singapore.
6
Department of Hematology, the First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
7
Department of Economics, National
University of Singapore, Singapore.
8
Department of Psychology, National University of Singapore, Singapore.
9
Division of Haematology and Laboratory Pathology, Tan
Tock Seng Hospital, Singapore.
10
Division of Medical Oncology, National Cancer Centre, Singapore.
11
Department of Dermatology, National Skin Centre, Singapore.
12
Department of Haematology-Oncology, National University Health System, National University of Singapore, Singapore.
13
Department of Haematology, Singapore
General Hospital, Singapore.
14
Department of Pathology, Singapore General Hospital, Singapore.
15
Department of Pathology, National University Health System,
National University of Singapore, Singapore.
16
Peking Union Medical College, Chinese Academy of Medical Science, Beijing, China.
17
Singapore Eye Research
Institute, Singapore.
18
Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
19
Department of Pediatrics,
Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
20
School of Biological Sciences, Anhui Medical University, Hefei, China.
21
Institute of Dermatology and Department of Dermatology, No.1 Hospital, Anhui Medical University, Hefei, China.
22
These authors contributed equally to this work.
23
These authors jointly directed this work. Correspondence should be addressed to J. Liu (liuj3@gis.a-star.edu.sg), W.-H.J. (jiawh@sysucc.org.cn),
A.L.H.S. (adeline_seow@nus.edu.sg) or D.L. (lindx72@cicams.ac.cn).
Received 19 October 2012; accepted 13 May 2013; published online 9 June 2013; doi:10.1038/ng.2666
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