698 VOLUME 18 | NUMBER 5 | MAY 2015 NATURE NEUROSCIENCE
ARTICLES
Schizophrenia is a devastating psychiatric disorder affecting 1% of
the population worldwide. The gene disrupted-in-schizophrenia 1
(DISC1) is a promising susceptibility factor for schizophrenia. The
DISC1 locus was originally identified at the breakpoint of a bal-
anced (1;11) (q42;q14) chromosome translocation that was found to
cosegregate with schizophrenia, bipolar disorder and recurrent major
depression in a large Scottish family
1,2
. Further analysis indicated that
inheritance of the translocation was causal and increased the risk of
these psychiatric disorders by 50-fold
1
.
To understand the molecular function of DISC1, several groups
have identified DISC1-interacting proteins, including nuclear dis-
tribution gene E homolog-like 1 (NDEL1), growth factor receptor-
bound protein 2 (GRB2), glycogen synthase kinase 3-β (GSK3β),
lissencephaly-1 (LIS1), kinesin family member 5B (KIF5B), fas-
ciculation and elongation protein-ζ 1 (FEZ1), girdin, kalirin and
phosphodiesterase 4B
3,4
. We previously reported that DISC1 is required
for the transport of some key regulators of axon outgrowth, including
the NDEL1–LIS1–14-3-3ε complex and GRB2 through the kinesin-1
motor complex
5,6
. These results indicate that DISC1 functions as
an adaptor molecule to link cargo molecules to kinesin-1 during
neurodevelopment. These efforts have provided a basis for examining
the processes and pathways affected by DISC1.
Studies carried out in vitro and in intact cells have shown that
DISC1 is involved in neurogenesis, neuronal migration, the formation
of axons and dendrites and synapse formation through inter-
actions with various partners
7
. We previously generated a Disc1-
knockout (Disc1
−/−
) mouse and developed a set of antibodies
to the N-terminal and C-terminal regions of DISC1 (DISC1n-Ab
and DISC1c-Ab, respectively)
8
. Disc1
−/−
mice revealed the follow-
ing problems in earlier DISC1 studies: (1) the presence of DISC1
isoforms, (2) the poor specificity of commercial antibodies to DISC1
and (3) the use of improper mouse strains as pointed out previously
9
.
DISC1n-Ab and DISC1c-Ab commonly detected a protein band of
100 kDa in a wild-type brain lysate but not in the Disc1
−/−
lysate.
Neither antibody detected any of the DISC1 isoforms postulated in
previous studies
10,11
, suggesting that the isoforms are not expressed
in the brain or that the expression levels are extremely low. When we
examined the specificity of the commercially available antibodies to
DISC1 used in previous studies
12–14
, we found that these antibodies
did not detect endogenous DISC1, presumably because of its low
abundance
8
. Gogos and others identified a 25-bp deletion in exon
6 of Disc1 in inbred 129 mice
15,16
. They claim that the micro-
deletion in Disc1 causes a frame shift and interferes with the
production of endogenous DISC1. We confirmed that the 129 and ICR
outbred mouse strains
8
, which were employed in the earlier DISC1
studies
14,17–19
, carried the same deletion and that these mouse strains
did not express DISC1. In the present study, it was reasonable to use
the Disc1
−/−
mouse to evaluate the physiological function of DISC1.
1
Department of Cell Pharmacology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi, Japan.
2
JST, CREST, Tokyo, Japan.
3
Department of Physiology,
Graduate School of Medicine, Nagoya University, Nagoya, Aichi, Japan.
4
Department of Biochemistry and Cellular Biology, National Institute of Neuroscience, Kodaira,
Tokyo, Japan.
5
Department of Anatomy and Cell Biology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi, Japan.
6
Department of Developmental and
Regenerative Biology, Graduate School of Medical Science, Nagoya City University, Nagoya, Aichi, Japan.
7
Department of Neural Regeneration and Cell Communication,
Mie University Graduate School of Medicine, Tsu, Mie, Japan.
8
Department of Neuronal Cell Biology, Okazaki Institute for Integrative Bioscience and National Institute
for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, Japan.
9
Department of Physiology, Keio University School of Medicine, Shinjuku, Tokyo,
Japan.
10
Brain Science Institute, RIKEN, Wako, Saitama, Japan. Correspondence should be addressed to K. Kaibuchi (kaibuchi@med.nagoya-u.ac.jp).
Received 19 December 2014; accepted 22 February 2015; published online 30 March 2015; doi:10.1038/nn.3984
Disrupted-in-schizophrenia 1 regulates transport of
ITPR1 mRNA for synaptic plasticity
Daisuke Tsuboi
1,2
, Keisuke Kuroda
1,2
, Motoki Tanaka
3
, Takashi Namba
1,2
, Yukihiko Iizuka
1,2
,
Shinichiro Taya
1,2,4
, Tomoyasu Shinoda
1,5
, Takao Hikita
1,6
, Shinsuke Muraoka
1
, Michiro Iizuka
2,7
,
Ai Nimura
1
, Akira Mizoguchi
7
, Nobuyuki Shiina
8
, Masahiro Sokabe
3
, Hideyuki Okano
9
, Katsuhiko Mikoshiba
10
& Kozo Kaibuchi
1,2
Disrupted-in-schizophrenia 1 (DISC1) is a susceptibility gene for major psychiatric disorders, including schizophrenia. DISC1 has
been implicated in neurodevelopment in relation to scaffolding signal complexes. Here we used proteomic analysis to screen for
DISC1 interactors and identified several RNA-binding proteins, such as hematopoietic zinc finger (HZF), that act as components
of RNA-transporting granules. HZF participates in the mRNA localization of inositol-1,4,5-trisphosphate receptor type 1 (ITPR1),
which plays a key role in synaptic plasticity. DISC1 colocalizes with HZF and ITPR1 mRNA in hippocampal dendrites and directly
associates with neuronal mRNAs, including ITPR1 mRNA. The binding potential of DISC1 for ITPR1 mRNA is facilitated by HZF.
Studies of Disc1-knockout mice have revealed that DISC1 regulates the dendritic transport of Itpr1 mRNA by directly interacting
with its mRNA. The DISC1-mediated mRNA regulation is involved in synaptic plasticity. We show that DISC1 binds ITPR1 mRNA
with HZF, thereby regulating its dendritic transport for synaptic plasticity.
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