LETTERS
NATURE CELL BIOLOGY VOLUME 8 | NUMBER 6 | JUNE 2006 615
Plexin-A1 and its interaction with DAP12 in immune
responses and bone homeostasis
Noriko Takegahara
1,12
, Hyota Takamatsu
1,12
, Toshihiko Toyofuku
1,2
, Tohru Tsujimura
3
, Tatsusada Okuno
4
,
Kazunori Yukawa
5
, Masayuki Mizui
1
, Midori Yamamoto
1
, Durbaka V.R. Prasad
1
, Kazuhiro Suzuki
1
, Masaru
Ishii
6
, Kenta Terai
7
, Masayuki Moriya
4
, Yuji Nakatsuji
4
, Saburo Sakoda
4
, Shintaro Sato
8
, Shizuo Akira
8
, Kiyoshi
Takeda
9
, Masanori Inui
10
, Toshiyuki Takai
10
, Masahito Ikawa
11
, Masaru Okabe
11
, Atsushi Kumanogoh
1,13
and
Hitoshi Kikutani
1,13
Semaphorins and their receptors have diverse functions in axon
guidance, organogenesis, vascularization and/or angiogenesis,
oncogenesis and regulation of immune responses
1–11
. The
primary receptors for semaphorins are members of the plexin
family
2,12–14
. In particular, plexin-A1, together with ligand-
binding neuropilins, transduces repulsive axon guidance
signals for soluble class III semaphorins
15
, whereas plexin-A1
has multiple functions in chick cardiogenesis as a receptor
for the transmembrane semaphorin, Sema6D, independent
of neuropilins
16
. Additionally, plexin-A1 has been implicated
in dendritic cell function in the immune system
17
. However,
the role of plexin-A1 in vivo, and the mechanisms underlying
its pleiotropic functions, remain unclear. Here, we generated
plexin-A1-deficient (plexin-A1
–/–
) mice and identified its
important roles, not only in immune responses, but also in bone
homeostasis. Furthermore, we show that plexin-A1 associates
with the triggering receptor expressed on myeloid cells-2 (Trem-
2), linking semaphorin-signalling to the immuno-receptor
tyrosine-based activation motif (ITAM)-bearing adaptor protein,
DAP12. These findings reveal an unexpected role for plexin-
A1 and present a novel signalling mechanism for exerting the
pleiotropic functions of semaphorins.
To better understand the role of plexin-A1 in vivo, mice deficient in
the plexin-A1 gene were generated by homologous recombination (see
Supplementary Information, Fig. S1a, b), and the successful deletion
of plexin-A1 was confirmed by both northern blotting and RT–PCR
(see Supplementary Information, Fig. S1c, d). Mice were born with the
expected Mendelian ratios from intercrosses of heterozygous mutants
and the resulting plexin-A1
–/–
mice were fertile. Apparent abnormalities
were not observed by gross macroscopic or histological examination
of the embryos (E11.5) or in the brain, kidney, lung, heart, liver and
spleen of 4-week-old mice — all tissues in which plexin-A1-transcripts
are expressed (see Supplementary Information, Fig. S1e, f). These obser-
vations strongly suggest the existence of functional redundancy among
the plexin family members during embryonic development. However,
mutant mice had functional defects in the immune system, as well as
morphologic abnormalities in the skeletal tissues. Therefore, the biologi-
cal functions of plexin-A1 were further investigated with a focus on the
immune and skeletal tissues as described below.
Lymphocyte development seemed to be normal in plexin-A1
–/–
mice.
No differences in the expression of cell surface phenotype markers,
numbers and ratios of T-cells, B-cells, macrophages and dendritic
cells in the spleen and thymus were observed between wild-type
and plexin-A1
–/–
mice (see Supplementary Information, Fig. S1g).
Plexin-A1 is highly expressed in dendritic cells
17
, and the influence
of plexin-A1-deficiency on dendritic cell function was examined.
FITC–dextran uptake by dendritic cells, and the appearance of fluo-
rescent dendritic cells in the draining lymph nodes after skin painting
with FITC, in plexin-A1
–/–
mice were comparable with those seen in
wild-type littermates (Fig. 1a, b). In addition, no significant differ-
ences were seen in the expression levels of costimulatory molecules
(including CD40, CD80, CD86 and MHC class II) between wild-
type and plexin-A1
–/–
dendritic cells (Fig. 1c). However, plexin-A1
–/–
1
Department of Molecular Immunology and CREST program of JST, Research Institute for Microbial Diseases, Osaka University, 3–1 Yamada-oka, Suita, Osaka 565-
0871, Japan.
2
Department of Internal Medicine and Therapeutics, Graduate School of Medicine, Osaka University, 2–2 Yamada-oka, Suita, Osaka 565–0871, Japan.
3
Department of Pathology, Hyogo College of Medicine, Hyogo 663–8501, Japan.
4
Department of Neurology, Graduate School of Medicine, Osaka University, 2–2 Yamada-
oka, Suita, Osaka 565–0871, Japan.
5
Department of Physiology II, Wakayama Medical College, 811–1 Kimiidera, Wakayama, Wakayama 641–0012, Japan.
6
Department
of Clinical Research, National Osaka Minami Medical Center, Kawachinagano, Osaka 586–8521, Japan.
7
Department of Signal Transduction, Research Institute for
Microbial Diseases, Osaka University, 3–1 Yamada-oka, Suita, Osaka 565–0871, Japan.
8
Department of Host Defence, Research Institute for Microbial Diseases, Osaka
University, and ERATO, Japan Science and Technology Agency, 3–1 Yamada-oka, Suita, Osaka 565–0871, Japan.
9
Department of Molecular Genetics, Medical Institute
for Bioregulation, Kyushu University, 3–1–1 Maidashi, Higashi-ku, Fukuoka 812–8582, Japan.
10
Department of Experimental Immunology, Institute of Development,
Aging and Cancer, Tohoku University, Siryo 4–1, Aoba-ku, Sendai 980–8575, Japan and CREST program of JST, Honcho 4–1–8, Kawaguchi, Saitama 332–0012, Japan.
11
Genome Information Research Center, Osaka University, 3–1 Yamada-oka, Suita, Osaka 565–0871, Japan.
12
These authors contributed equally to this work.
13
Correspondence should be addressed to A.K. and H.K. (e-mail: kumanogo@ragtime.biken.osaka-u.ac.jp; kikutani@ragtime.biken.osaka-u.ac.jp)
Received 21 February 2006; accepted 28 April 2006; published online 21 May 2006; DOI: 10.1038/ncb1416
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