ARTICLES
Rheumatoid arthritis is a chronic inflammatory disease with
autoimmune features that affects 0.5–1.0% of the world’s popula-
tion including the Japanese. Although the precise etiology of
rheumatoid arthritis is unknown, genetic and environmental fac-
tors seem to be involved in its pathogenesis. The relative risk of
developing the disorder is 2–17 times higher in siblings of affected
individuals as compared to the general population, implying a
genetic contribution to rheumatoid arthritis susceptibility
1
. Several
genes are thought to contribute to susceptibility to rheumatoid
arthritis
2–6
.
As an alternative to linkage studies
4,6–8
and approaches based on
target genes, LD mapping with SNPs for candidate regions coupled
with whole-genome screening is considered to be a useful method for
genetic association studies
9,10
. To identify genes associated with
rheumatoid arthritis, a whole-genome LD mapping study using a
high-throughput multiplex PCR-Invader assay
11,12
is currently in
progress. Although incomplete, this project has previously identified
the gene encoding peptidylarginine deiminase type IV as being asso-
ciated with susceptibility to rheumatoid arthritis
13
.
Inflammation of the synovium is one of the primary pathological
features of rheumatoid arthritis. It is characterized by an increase in
the number of inflammatory cells and the formation of granulation
tissue with the subsequent destruction of joints. Autoimmunity is
also considered to have an important role in the pathogenesis of
rheumatoid arthritis because various autoantibodies are produced in
conjunction with manifestations of rheumatoid arthritis
14
. The chro-
mosomal region 5q31 is of particular interest in rheumatoid arthritis
because it contains many genes involved in immune and inflamma-
tory systems and also because it is suggested to be a susceptibility
locus for several inflammatory or autoimmune diseases, including
Crohn disease, atopic dermatitis and bronchial asthma, by studies on
humans and mice
15–19
. For these reasons, we focused our search for
genes associated with rheumatoid arthritis on the 5q31 cytokine clus-
ter region using LD mapping with SNPs.
We report here that the gene encoding solute carrier family 22,
member 4 (SLC22A4) on chromosome 5q31 is associated with
rheumatoid arthritis. SLC22A4 has been reported as encoding a
transporter of organic molecules, and a region spanning 250 kb that
1
Laboratory for Rheumatic Diseases, SNP Research Center, The Institute of Physical and Chemical Research (RIKEN), 1-7-22, Suehiro-cho, Tsurumi-ku, Yokohama
City, Kanagawa 230-0045, Japan.
2
Sankyo, Tokyo, Japan.
3
Department of Allergy and Rheumatology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan.
4
Department of Joint Disease and Rheumatism, Nippon Medical School, Tokyo, Japan.
5
Laboratory for Bone and Joint Diseases, SNP Research Center, The Institute
of Physical and Chemical Research (RIKEN), Tokyo, Japan.
6
Laboratory for Genotyping, SNP Research Center, The Institute of Physical and Chemical Research
(RIKEN), Kanagawa, Japan.
7
Laboratory for Medical Informatics, SNP Research Center, The Institute of Physical and Chemical Research (RIKEN), Kanagawa, Japan.
8
Laboratory of Molecular Medicine, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo, Japan.
9
Research Group for Personalized
Medicine, SNP Research Center, The Institute of Physical and Chemical Research (RIKEN), Tokyo, Japan. Correspondence should be addressed to R.Y.
(ryamada@src.riken.go.jp).
Published online 9 November 2003; doi:10.1038/ng1267
An intronic SNP in a RUNX1 binding site of SLC22A4,
encoding an organic cation transporter, is associated with
rheumatoid arthritis
Shinya Tokuhiro
1,2
, Ryo Yamada
1
, Xiaotian Chang
1
, Akari Suzuki
1
, Yuta Kochi
1,3
, Tetsuji Sawada
3
, Masakatsu Suzuki
2
,
Miyuki Nagasaki
2
, Masahiko Ohtsuki
2
, Mitsuru Ono
2
, Hidehiko Furukawa
2
, Masakazu Nagashima
4
,
Shinichi Yoshino
4
, Akihiko Mabuchi
5
, Akihiro Sekine
6
, Susumu Saito
6
, Atsushi Takahashi
7
, Tatsuhiko Tsunoda
7
,
Yusuke Nakamura
8,9
& Kazuhiko Yamamoto
1,3
Rheumatoid arthritis is a common inflammatory disease with complex genetic components. We investigated the genetic
contribution of the cytokine gene cluster in chromosome 5q31 to susceptibility to rheumatoid arthritis in the Japanese
population by case-control linkage disequilibrium (LD) mapping using single nucleotide polymorphisms (SNPs). Here we
report that there is significant association between rheumatoid arthritis and the organic cation transporter gene SLC22A4
(P = 0.000034). We show that expression of SLC22A4 is specific to hematological and immunological tissues and that SLC22A4
is also highly expressed in the inflammatory joints of mice with collagen-induced arthritis. A SNP affects the transcriptional
efficiency of SLC22A4 in vitro, owing to an allelic difference in affinity to Runt-related transcription factor 1 (RUNX1), a
transcriptional regulator in the hematopoietic system. A SNP in RUNX1 is also strongly associated with rheumatoid arthritis
(P = 0.00035). Our data indicate that the regulation of SLC22A4 expression by RUNX1 is associated with susceptibility to
rheumatoid arthritis, which may represent an example of an epistatic effect of two genes on this disorder.
NATURE GENETICS VOLUME 35 | NUMBER 4 | DECEMBER 2003 341
© 2003 Nature Publishing Group http://www.nature.com/naturegenetics