Association of Tyrosine Phosphatases SHP-1 and SHP-2,
Inositol 5-Phosphatase SHIP with gp49B1, and Chromosomal
Assignment of the Gene*
Asato
Kuroiwa,
Yumi
Yamashita
§,
Masanori
Inui
¶,
Takae
Yuasa
§¶,
Masao
Ono
§¶,
Akira
Nagabukuro,
Yoichi
Matsuda, and
Toshiyuki
Takai
§¶
From the Laboratory of Animal Genetics, School of Agricultural
Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-01,
Department of Biotechnology, Faculty of Engineering,
Okayama University, Tsushima-Naka, Okayama 700, and § Core
Research for Evolutional Science and Technology (CREST), Japan Science
and Technology Corporation, Japan
 |
ABSTRACT |
We have analyzed the molecules participating in
the inhibitory function of gp49B1, a murine type I transmembrane
glycoprotein expressed on mast cells and natural killer cells, as well
as the chromosomal location of its gene. As assessed by
SDS-polyacrylamide gel electrophoresis and immunoblot analysis,
tyrosine-phosphorylated, but not nonphosphorylated, synthetic peptides
matching each of the two immunoreceptor tyrosine-based inhibitory motif
(ITIM)-like sequences found in the cytoplasmic portion of gp49B1
associated with the ~65-kDa tyrosine phosphatase SHP-1 and ~70-kDa
SHP-2 derived from RBL-2H3 cells. In addition, the phosphotyrosyl
peptide matching the second ITIM-like sequence also bound the
~145-kDa inositol polyphosphate 5-phosphatase SHIP. Thus, it has been
strongly suggested that the inhibitory nature of gp49B involves the
recruitment of SHP-1, SHP-2, and SHIP for the delivery of inhibitory
signal to the cell interior upon phosphorylation of tyrosine residues in their ITIMs. The gp49B gene has been found to be in the
juxtaposition of its cognate gene, gp49A. The gene pair was shown to
locate in the B4 band of mouse chromosome 10. In this region, no
conserved linkage homology to human chromosome 19, where the genes for
killer cell inhibitory receptors are found, has been identified.
 |
INTRODUCTION |
The immunoreceptor tyrosine-based inhibitory motif
(ITIM)1 is a set of amino
acid sequences that deliver an inhibitory signal upon phosphorylation
of the specific tyrosine residues. The motif is found in cytoplasmic
portions of Fc
RIIB (1-3), CD22 (4, 5), and inhibitory receptors
expressed by human and mouse natural killer (NK) cells (6). The
consensus sequence of ITIM is
(V/I)-X-Y-X-X-(L/V) (7). In B cells,
when F(ab
)2 fragments of anti-membrane immunoglobulin antibody induce cross-linkage of the surface B cell antigen receptors, a signal transduction cascade is elicited through the receptor that
results in B cell proliferation and differentiation into antibody-producing cells. In contrast, stimulation with intact anti-membrane Ig antibody results in co-cross-linkage between the B
cell antigen receptor and Fc
RIIB, in attenuated B cell signal
transduction due to the phosphorylation of ITIM of Fc
RIIB, and
binding of src homology 2 (SH2)-containing proteins, which inhibit calcium signaling pathway (2, 3). The importance of the
inhibitory nature of Fc
RIIB in the humoral immune response in
vivo was demonstrated in the Fc
RIIB-deficient mice generated by
gene targeting (8). The proteins to be associated with the phosphorylated ITIM sequence of Fc
RIIB was verified to be an SH2-containing tyrosine phosphatase, SHP-1 (9), and an SH2-containing inositol polyphosphate 5-phosphatase, SHIP, in B cells, whereas in mast
cells SHIP was shown to be preferentially recruited (10).
On the other hand, human and mouse NK cells express two kinds of
inhibitory molecules containing ITIMs. One of which, human killer cell
inhibitory receptor (KIR), is a type I transmembrane glycoprotein
belonging to Ig superfamily (6, 11, 12). In contrast, human CD94 and
mouse Ly-49 molecules are type II transmembrane glycoprotein with
C-type lectin structure (13, 14). Despite these quite different
structures, both Ly-49 and KIR recognize allelic groups of the major
histocompatibility complex class I molecules on target cells.
Engagement of these inhibitory receptors results in a dominant negative
signal that prevents lysis of the target cells. Tyrosine
phosphorylation of their ITIMs and recruitment of SHP-1 was shown to be
critical for the inhibitory function (7, 15).
Recently, it was shown that mouse NK cells as well as mast cells also
express KIR-like molecules, gp49A (16) and gp49B1 (17), the latter of
which contains two ITIM-like sequences in its cytoplasmic portion
(17-21). Although the physiological function of gp49 molecules is
unknown, it was demonstrated that the co-ligation of gp49B1 and a high
affinity IgE receptor Fc
RI on the surface of mast cells suppresses
Fc
RI-mediated exocytosis, suggesting that this molecule possibly
functions as an inhibitory receptor (19). Moreover, transfection
experiments have indicated that the cytoplasmic tail of gp49B1 inhibits
lysis of major histocompatibility complex class I-negative cell line by
mouse and human NK cell lines, showing the inhibitory nature of the
gp49B1 molecule in NK cells (20). Thus, elucidation of the
physiological ligand for gp49 as well as the biochemical
characteristics of the inhibitory cascade of the molecule should be
valuable for understanding the mode of action that regulates activating
and inhibitory signaling in cells of the immune system.
We report here that both of the phosphorylated ITIM-like sequences of
gp49B1 bind SHP-1 and SHP-2, whereas the phosphotyrosyl second
ITIM-like sequence associates with SHIP from RBL-2H3 cells. Moreover,
we found that the gp49B gene and the cognate gp49A gene are
co-localized on the B4 region of mouse chromosome 10, which is
apparently not a syntenic position of human chromosome 19, where genes
for the KIR family are present (6, 22).
 |
EXPERIMENTAL PROCEDURES |
Screening and Isolation of Mouse Genomic DNA Clones for
gp49B--
A 1.0-kilobase pair (kbp) cDNA of gp49B was prepared by
reverse transcription-polymerase chain reaction (PCR) of mRNA
preparation from WEHI-3 cells using an oligo(dT) primer for a reverse
transcription reaction, and the forward primer
(5
-CGATAAGCTTGCCTGGACTCACCATG-3
) corresponding to nucleotide residues
7-24 (17) containing a HindIII restriction site, and the
backward primer (5
-CGATGGATCCCTAGTTTTCATTCATGG-3
) corresponding to
the residues 1075-1095 of gp49B1 containing a BamHI
restriction site for a PCR reaction. After the PCR amplification and
digestion with HindIII and BamHI, the gp49B
cDNA was cloned into the HindIII/BamHI sites
of pUC19. The cDNA insert was labeled with random primer labeling
kit (Takara Shuzo Co., Otsu, Japan) and [
-32P]dCTP
(specific activity, ~3,000 Ci/mmol, Amersham Corp.), and was used to
screen a 129/Sv mouse genomic library (Stratagene): 8.3 × 105 plaques were screened under stringent conditions (23).
The resulting two positive clones were plaque-purified, and they were subcloned into the plasmid pUC19 or pBluescript (Stratagene) and sequenced by the dideoxy chain termination method (24) using a Cy5
AutoRead sequencing kit and an ALFexpress DNA sequencer (both from
Pharmacia Biotech Inc.).
Cell Culture--
Bone marrow-derived mast cells from C57BL/6 or
B10.A mice were prepared as described previously (25). RBL-2H3 cells
(obtained from the Japanese Cancer Research Resources Bank, Tokyo) were maintained in RPMI 1640 plus 10% fetal calf serum.
Affinity Isolation of Cellular Proteins and Immunoblot
Analysis--
For the detection of cellular proteins that bind to two
ITIM-like sequences found in the cytoplasmic portion of gp49B, four biotinylated peptides were synthesized: the sequences are
DPQGIVYAQVKP-amide (in one-letter code, designated as Y1, corresponding
to amino acid residues 294-305, see Ref. 17), DPQGIV(pY)AQVKP-amide
(pY1), ETQDVTYAQLCI-amide (Y2, residues 316-327), and
ETQDVT(pY)AQLCI-amide (pY2), where each N-terminal residue is
biotinylated, and (pY) denotes a phosphotyrosine residue.
RBL-2H3 cells and bone marrow-derived mast cells were solubilized by
adding extraction buffer (50 mM Tris-HCl, pH 7.4, 1% Nonidet P-40, 150 mM NaCl, 1 mM phenylmethyl
sulfonyl fluoride, 10 µg/ml aprotinin, 20 µg/ml leupeptin, 1 mM disodium EDTA, 10% glycerol) to the cell pellet. The
extract was then incubated on ice for 10 min, and the insoluble
material was removed by centrifugation at 15,000 × g
for 15 min at 4 °C. The soluble extract was precleared with 1.0 ml
of avidin-Sepharose FF beads/107 cell eq (Pharmacia) in
extraction buffer. The beads were removed by centrifugation at
15,000 × g for 5 min, and the extract was then
incubated for 18 h at 4 °C with 0.5 ml of the biotinylated peptide avidin-Sepharose beads/107 cell eq, followed by
precipitation. The pelleted beads were washed four times by
centrifugation in extraction buffer containing 0.1% gelatin and devoid
of aprotinin and leupeptin, resuspended in sodium dodecyl
sulfate-polyacrylamide gel electrophoresis sample buffer (50 mM Tris-HCl, pH 6.8, 2% SDS, 0.1% bromphenol blue, 10%
glycerol, and 150 mM 2-mercaptoethanol), boiled for 1 min to liberate immunoprecipitated materials, and centrifuged. The affinity-isolated materials or cell lysates were subjected to SDS-polyacrylamide gel electrophoresis separation using 7.5% gel and
then transferred to a polyvinylidine difluoride membrane (Immobilon P,
Millipore Corp.) using a Milliblot electroblotting system. The blot was
first blocked with 2% nonfat dry milk (Carnation) in
phosphate-buffered saline, 0.05% Tween 20, incubated with 0.5 µg/ml
rabbit anti-SHP-1 or anti-SHP-2 IgG (both from Santa Cruz Biotechnology, Santa Cruz, CA), or rabbit anti-SHIP antiserum (generously provided by Dr. K. M. Coggeshall, Ohio State
University) and washed three times in phosphate-buffered saline/Tween.
The blot was then treated with the peroxidase-conjugated mouse
anti-rabbit IgG (clone RG-16, Sigma) and detected by enhanced
chemiluminescence (Amersham Corp.).
Chromosome Preparation and in Situ Hybridizaiton--
The direct
R-banding fluorescence in situ hybridization method was used
for chromosomal assignment of the mouse gp49B gene. Preparation of
R-banded chromosomes and fluorescence in situ hybridization were performed as described by Matsuda et al. (26) and
Matsuda and Chapman (27). The chromosome slides were hardened at
65 °C for 2 h, denatured at 70 °C in 70% formamide in
2 × SSC, and dehydrated in cold ethanol (5 min each in 70 and
100%).
The mouse 6.7-kb genomic DNA fragment inserted in SacI site
of pBluescript were labeled by nick translation with biotin 16-dUTP (Boehringer Mannheim) following the manufacturer's protocol. The labeled DNA fragment was ethanol-precipitated with a 10-fold excess of
mouse Cot-1 DNA (Life Technologies, Inc.), sonicated salmon sperm DNA
and E. coli tRNA, and then denatured at 75 °C for 10 min
in 100% formamide. The denatured probe was mixed with an equal volume
of hybridization solution to make final concentration of 50%
formamide, 2 × SSC, 10% dextran sulfate, and 2 mg/ml bovine serum albumin (Sigma). The mixed probe was placed on the denatured chromosome slides and incubated overnight at 37 °C. The slides were
washed in 50% formamide in 2 × SSC at 37 °C for 20 min and in
2 × SSC and 1 × SSC for 20 min each at room temperature.
After rinsing in 4 × SSC, they were incubated under coverslips
with fluoresceinated avidin (Vector Laboratories) at a 1:500 dilution in 1% bovine serum albumin, 4 × SSC for 1 h at 37 °C.
They were washed sequentially with 4 × SSC, 0.1% Nonidet P-40 in
4 × SSC and 4 × SSC for 10 min each on a shaker, rinsed
with 2 × SSC, and stained with 0.75 µg/ml propidium iodide
(Sigma). Excitation at wavelength 450-490 nm (Nikon filter set B-2A)
and near 365 nm (UV-2A) was used for observation. Kodak Ektachrome ASA
100 films were used for microphotography.
Linkage Mapping with Interspecific Backcross
Mice--
Recombinant mice used in this study were generated by mating
male feral-derived mouse stocks, Mus spretus, with female
C57BL/6J, and backcrossing the F1 female with male M. spretus (28). Genomic DNA derived from kidneys of each backcross
mouse was digested with restriction endonucleases. The resulting
fragments were separated on 0.8% agarose gels and transferred to a
nylon membrane (Bio-Rad). The DNA was used to determine the genotype of
each animal by Southern blot hybridization following the standard
protocol. According to the result obtained by the cytogenetic mapping
using fluorescence in situ hybridization, microsatellite DNA
markers (Research Genetics, Huntsville, AL) for linkage analysis were
chosen. All PCR reactions were performed in a total 15-µl reaction
mixture containing 125 ng genomic DNA and 15 pmol oligonucleotide
primers. Amplification conditions were 95 °C for 10 min, 30 cycles
of 94 °C for 1 min, 55 °C for 1 min, and 72 °C for 50 s,
and 72 °C for 10 min. The PCR products were visualized under UV
light with ethidium bromide staining after separation on polyacrylamide
gel.
 |
RESULTS AND DISCUSSION |
Analysis of Cellular Components Associating with Cytoplasmic Domain
of gp49B--
gp49B has two possible ITIM sequences in its 74-amino
acid cytoplasmic domain (17-19). One is IVYAQV, and the other is
VTYAQL: they are separated by 18 amino acid residues. On the other
hand, its cognate molecule gp49A has a short cytoplasmic region
comprised of 42 amino acid residues, and has no such inhibitory
sequences within this region (16). Transfection experiments have shown that the whole cytoplasmic portion of gp49B is sufficient for the
inhibitory nature of the gp49B molecule in NK cells (20). A question
arises whether the possible ITIM sequences of gp49B actually function
as inhibitory motifs that interact with any cellular component or not.
To address this issue, we attempted to detect cellular proteins
associating with these sequences. Cellular proteins of RBL-2H3 cells
and bone marrow-derived mast cells were lysed and then incubated with
tyrosine-phosphorylated or nonphosphorylated synthetic peptide matching
each ITIM-like sequence found in the cytoplasmic portion of gp49B. The
bound proteins were separated by SDS-polyacrylamide gel electrophoresis and subjected to immunoblot analysis. As shown in Fig.
1, both anti-SHP-1 and anti-SHP-2
antibodies detected a ~65- and ~70-kDa protein, respectively, bound
to pY1 and pY2 but not to the corresponding nonphosphotyrosyl peptides.
Unexpectedly, we found that anti-SHIP antiserum clearly detected a
~145-kDa protein associating with pY2 but not with pY1 and the
corresponding nonphosphotyrosyl peptides. Detection of possible
association of Syk kinase using anti-Syk antiserum was not successful
(data not shown). Therefore, we concluded that each phosphorylated
ITIM-like sequence mainly binds SHP-1 and SHP-2, whereas the second
possible ITIM also associates with SHIP from RBL-2H3 extract.
Inhibition of cellular activation signal by SHP-1 is associated with
inhibition of early tyrosine phosphorylation events, release of
Ca2+ from intracellular stores, and secondary influx of
extracellular Ca2+. On the other hand, SHIP inhibits only
the secondary influx of extracellular Ca2+. Thus, we
postulate that the two possible ITIM sequences in gp49B can function as
inhibitory motifs within the cells. Since the recruitment of SHP-1,
SHP-2 and SHIP is dependent on the presence of the phosphotyrosine
residue, the phosphorylation of specific tyrosine residues in ITIM-like
sequences of gp49B should be prerequisite for recruitment of SHP-1 and
SHIP in stimulated cells such as mast cells. Since the gp49-specific
antibody is not available at present, we cannot verify that the
cytoplasmic tail of gp49B is tyrosine-phosphorylated within the cells.
Possible candidates that phosphorylate the tyrosine residues in the
cytoplasmic domain of gp49B are a src family kinase or a
Syk/Zap-70 family kinase such as Lyn or Syk, but this issue remains to
be clarified. A possibility remains that the preference of the
association with SHP-1 or SHIP could be dependent on the cell type.

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Fig. 1.
Association of SHP-1, SHP-2, and SHIP with
phosphotyrosyl ITIM-like sequences of gp49B1. RBL-2H3 cell lysate
was adsorbed with the indicated peptides. Affinity bound proteins were
resolved on 7.5% SDS-polyacrylamide gel electrophoresis and probed
with rabbit anti-SHIP antiserum, anti-SHP-1 IgG, or anti-SHP-2 IgG. Mock, mock affinity isolation without any peptide but with
avidin-Sepharose; Lysate, total cell lysate without any
adsorption.
|
|
Juxtaposition of gp49A and gp49B Genes--
As mentioned above,
two related genes have been identified for mouse gp49, gp49A and gp49B,
by cloning of cDNA for each molecule (16, 17), cloning of genomic
DNA for gp49B (17), and blot hybridization analysis of total genomic
DNA (16). Recently, several groups of genes with almost the same
structural characteristics but different in their cytoplasmic regions
are revealed. One example is a group of KIR that comprises inhibitory
KIR molecules and the molecules with nearly the same extracellular
domains but with no inhibitory cytoplasmic domains such as some of the
NK-associated transcripts (for review, see Refs. 29-32). The genes for
them have been found to be clustered in human chromosome 19q13 (22).
Therefore, it is interesting to test a hypothesis that gp49 genes also
locate in a limited area of a mouse chromosome.
The first step toward this issue, we have isolated the genomic clones
for gp49B using a gp49B cDNA fragment as a probe. We initially
characterized the exon/intron structures of one of the positive clones
(clone 1, harboring a 16-kb insert and containing all of the exons for
gp49B). Unexpectedly, we found that this genomic clone 1 also contained
a 3
part of the gene for gp49A as shown in Fig.
2. An overlapping clone, clone 2, was
also shown to contain all of the gp49A exons and a 5
part of the gene
for gp49B by sequencing analysis. Thus, we found that gp49A and gp49B genes are in the juxtaposition and in the same orientation: they are
apart by 4.4 kb (Fig. 2). In addition, sequencing analysis of the gp49A
and gp49B genes from 129/Sv mouse revealed that there is no nucleotide
substitution in the exon sequences when compared with the respective
genes from BALB/c and C3H mice, respectively (data not shown),
supporting the notion that gp49 genes are not polymorphic within a
species.

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Fig. 2.
Co-localization of genes for gp49A and gp49B
within a 17-kb area of mouse genome. Schematic representation of
the exon/intron structures of gp49A and gp49B genes is shown. The
protein-coding sequences are denoted as closed boxes, and
the noncoding sequences are open boxes.
|
|
Chromosomal Mapping of the gp49B Gene--
The chromosomal
assignment of the mouse gp49B gene was performed by direct R-banding
fluorescence in situ hybridization using a mouse genomic DNA
fragment as a biotinylated probe. As shown in Fig.
3, the signals of the gp49B gene were
detected on the R-band-positive B4 band of mouse chromosome 10 (33).

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Fig. 3.
Chromosomal localization of the gp49B gene on
mouse R-banded chromosomes. The chromosomal location of the mouse
gp49B gene was determined by using a 6.7-kb genomic DNA fragment as a
biotinylated probe. The hybridization signals are indicated by
arrows. The signals are located on mouse chromosome 10B4.
The metaphase spreads were photographed with a Nikon B-2A (panels a and c) and UV-2A (b) filters. R-band and
G-band patterns are demonstrated in panels a and
c and panel b, respectively.
|
|
For fine linkage mapping of the mouse gp49B gene, genomic DNAs of
C57BL/6J, M. spretus and their F1 were digested
with six different restriction endonucleases to find the restriction
fragment length variants using Southern blot hybridization. The
restriction fragment length variant with HindIII, 6.1 kb in
C57BL/6J and 5.4 kb in M. spretus, was used to examine the
concordance of segregation of the restriction fragment length variant
with the segregation of microsatellite markers, D10Mit3,
D10Mit38, D10Mit20, D10Mit31, and
D10Mit7. Gene order was determined by minimizing the number of multiple recombinations among the loci on the same chromosome. Comparative pairwise loci analyses showed the gene order and
recombination frequency for gp49B on mouse chromosome 10 (genetic
distance in centimorgan ± S.E. and the number of recombinations
in parentheses) as follows: centromere, D10Mit3, 3.5 ± 2.0 (3/86), D10Mit38, 3.5 ± 2.0 (3/86),
gp49B, 1.2 ± 1.2 (1/86), D10Mit20, 3.5 ± 2.0 (3/86), D10Mit31, 10.5 ± 3.3 (9/86),
D10Mit7, telomere (Fig. 4). It
should be emphasized that the conserved linkage homology to human
chromosome 19, where KIR genes have been localized, has not been
identified in this region.

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Fig. 4.
Location of gp49 locus on mouse
chromosome 10. A, the segregation patterns of the mouse
gp49B gene with flanking eight microsatellite DNA markers,
D10Mit3, D10Mit38, D10Mit20, D10Mit31, and
D10Mit7, in the backcross mice are shown. Each column
represents the chromosome identified in the backcross progeny that was
inherited from the (C57BL/6 × M. spretus)F1 parent. represent the presence of
M. spretus allele, and represent the presence of C57BL/6 allele. The number of offspring inheriting each type of chromosome is
listed at the bottom of each column. B, the partial
chromosome 10 linkage map shows the location of mouse gp49B
locus in relation to the flanking DNA markers. Recombination distances
between loci are shown in centimorgan to the right of the
chromosome.
|
|
Recent progress in structural and functional aspects of KIR have
proposed an intriguing hypothesis that there may be several unidentified groups of molecules with positive and negative regulatory functions in human as well as in mouse. In fact, human
immunoglobulin-like transcript-1, -2, and -3 (34, 35), mouse gp49A and
gp49B (17-21), and mouse p91 (36) and paired inhibitory receptors (37)
are candidates for such regulatory groups or pairs that may play
important roles in the initiation of cellular responses. In this
report, we showed that the cytoplasmic ITIM sequences of gp49B1 are
able to recruit SHP-1, SHP-2, and SHIP upon tyrosine phosphorylation, suggesting that the inhibitory function of gp49B1 is due to the recruitment of these phosphatases to the phosphorylated ITIM and inhibiting the activation signaling such as the increase in the intracellular Ca2+ concentration. Studies on the ligand and
activatory/inhibitory signaling cascades of gp49 molecules will
facilitate the understanding of the mode of regulation of cells in the
immune system.
 |
FOOTNOTES |
*
This work was supported by research grants from the Ministry
of Education, Science, Sports, and Culture of Japan (to Y. M. and
T. T.), and Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation (to T. T.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
¶
Present address: Laboratory of Molecular Embryology, Institute
of Development, Aging, and Cancer, Tohoku University, Seiryo 4-1, Sendai 980-77, Japan. To whom correspondence should be addressed. Tel.:
81-22-717-8501; Fax: 81-22-717-8505; E-mail:
tostakai{at}idac.tohoku.ac.jp.
1
The abbreviations used are: ITIM, immunoreceptor
tyrosine-based inhibitory motif; bp, base pair(s); Fc
R, IgG Fc
receptor; kbp, kilobase pair(s); KIR, killer cell inhibitory
receptor; NK, natural killer; PCR, polymerase chain reaction; SH2,
src homology 2; SHIP, SH2-containing inositol polyphosphate
5-phosphatase; SHP, SH2-containing tyrosine phosphatase.
 |
REFERENCES |
-
Daeron, M.,
Latour, S.,
Malbec, O.,
Espinosa, E.,
Pina, P.,
Pasmans, S.,
and Fridman, W. H.
(1995)
Immunity
3,
635-646[Medline]
[Order article via Infotrieve]
-
Amigorena, S.,
Bonnerot, C.,
Drake, J. R.,
Choquet, D.,
Hunziker, W.,
Guillet, J. G.,
Webster, P.,
Sautes, C.,
Mellman, I.,
Fridman, W. H.
(1992)
Science
256,
1808-1812[Medline]
[Order article via Infotrieve]
-
Muta, T.,
Kurosaki, T.,
Misulovin, Z.,
Sanchez, M.,
Nussenzweig, M. C.,
Ravetch, J. V.
(1994)
Nature
368,
70-73[CrossRef][Medline]
[Order article via Infotrieve]
-
Thomas, M. L.
(1995)
J. Exp. Med.
181,
1953-1956[Medline]
[Order article via Infotrieve]
-
Doody, G. M.,
Justement, L. B.,
Delibrias, C. C.,
Matthews, R. J.,
Lin, J.,
Thomas, M. L.,
Fearon, D. T.
(1995)
Science
269,
242-244[Medline]
[Order article via Infotrieve]
-
Wagtmann, N.,
Biassoni, R.,
Cantoni, C.,
Verdiani, S.,
Malnati, M. S.,
Vitale, M.,
Bottino, C.,
Moretta, L.,
Moretta, A.,
Long, E. O.
(1995)
Immunity
2,
439-449[Medline]
[Order article via Infotrieve]
-
Burshtyn, D. N.,
Scharenberg, A. M.,
Wagtmann, N.,
Rajagopalan, S.,
Berrada, K.,
Yi, T.,
Kinet, J.-P.,
Long, E. O.
(1996)
Immunity
4,
77-85[Medline]
[Order article via Infotrieve]
-
Takai, T.,
Ono, M.,
Hikida, M.,
Ohmori, H.,
and Ravetch, J. V.
(1996)
Nature
379,
346-349[CrossRef][Medline]
[Order article via Infotrieve]
-
D'Ambrosio, D.,
Hippen, K. L.,
Minskoff, S. A.,
Mellman, I.,
Pani, G.,
Siminovitch, K. A.,
Cambier, J. C.
(1995)
Science
268,
293-297[Medline]
[Order article via Infotrieve]
-
Ono, M.,
Bolland, S.,
Tempst, P.,
and Ravetch, J. V.
(1996)
Nature
383,
263-266[CrossRef][Medline]
[Order article via Infotrieve]
-
Colonna, M.,
and Samaridis, J.
(1995)
Science
268,
405-408[Medline]
[Order article via Infotrieve]
-
D'Andrea, A.,
Chang, C.,
Franz-Bacon, K.,
McClanahan, T.,
Phillips, J.,
and Lanier, L. L.
(1995)
J. Immunol.
155,
2306-2310[Abstract]
-
Chang, C.,
Rodriguez, A.,
Carretero, M.,
Lopez-Botet, M.,
Phillips, J. H.,
Lanier, L. L.
(1995)
Eur. J. Immunol.
25,
2433-2437[Medline]
[Order article via Infotrieve]
-
Yokoyama, W. M.,
and Seaman, W. E.
(1993)
Annu. Rev. Immunol.
11,
613-635[CrossRef][Medline]
[Order article via Infotrieve]
-
Campbell, K. S.,
Dessing, M.,
Lopez-Botet, M.,
Cella, M.,
and Colonna, M.
(1996)
J. Exp. Med.
184,
93-100[Abstract]
-
Arm, J. P.,
Gurish, M. F.,
Reynolds, D. S.,
Scott, H. C.,
Gartner, C. S.,
Austen, K. F.,
Katz, H. R.
(1991)
J. Biol. Chem.
266,
15966-15973[Abstract/Free Full Text]
-
Castells, M. C.,
Wu, X.,
Arm, J. P.,
Austen, K. F.,
Katz, H. R.
(1994)
J. Biol. Chem.
269,
8393-8401[Abstract/Free Full Text]
-
Katz, H. R.,
and Austen, K. F.
(1997)
J. Immunol.
158,
5065-5070[Abstract]
-
Katz, H. R.,
Vivier, E.,
Castells, M. C.,
McCormick, M. J.,
Chambers, J. M.,
Austen, K. F.
(1996)
Proc. Natl. Acad. Sci. U. S. A.
93,
10809-10814[Abstract/Free Full Text]
-
Rojo, S.,
Burshtyn, D. N.,
Long, E. O.,
Wagtmann, N.
(1997)
J. Immunol.
158,
9-12[Abstract]
-
Wang, L. L.,
Mehta, I. K.,
LeBlanc, P. A.,
Yokoyama, W. M.
(1997)
J. Immunol.
158,
13-17[Abstract]
-
Baker, E.,
D'Andrea, A.,
Phillips, J. H.,
Sutherland, G. R.,
Lanier, L. L.
(1995)
Chromosome Res.
3,
511
-
Sambrook, J.,
Fritsch, E. F.,
and Maniatis, T.
(1989)
Molecular Cloning: A Laboratory Manual, 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
-
Sanger, F.,
Nicklen, S.,
and Coulson, A. R.
(1977)
Proc. Natl. Acad. Sci. U. S. A.
74,
5463-5467[Abstract]
-
Takai, T.,
Li, M.,
Sylvestre, D.,
Clynes, R.,
and Ravetch, J. V.
(1994)
Cell
76,
519-529[Medline]
[Order article via Infotrieve]
-
Matsuda, Y.,
Harada, Y.-N.,
Natsuume-Sakai, S.,
Lee, K.,
Shiomi, T.,
and Chapman, V. M.
(1992)
Cytogenet. Cell Genet.
61,
282-285[Medline]
[Order article via Infotrieve]
-
Matsuda, Y.,
and Chapman, V. M.
(1995)
Electrophoresis
16,
261-272[Medline]
[Order article via Infotrieve]
-
Matsuda, Y.,
Imai, T.,
Shiomi, T.,
Saito, T.,
Yamauchi, M.,
Fukao, T.,
Akao, Y.,
Seki, N.,
Ito, T.,
and Hori, T.
(1996)
Genomics
34,
347-357[CrossRef][Medline]
[Order article via Infotrieve]
-
Leibson, P. J.
(1997)
Immunity
6,
655-661[Medline]
[Order article via Infotrieve]
-
Long, E. O.,
and Burshtyn, D. N.
(1997)
Immunol. Rev.
155,
135-144[Medline]
[Order article via Infotrieve]
-
Lanier, L. L.,
and Phillips, J. H.
(1996)
Immunol. Today
17,
86-91[CrossRef][Medline]
[Order article via Infotrieve]
-
Raulet, D. H.,
and Held, W.
(1995)
Cell
82,
697-700[CrossRef][Medline]
[Order article via Infotrieve]
-
Evans, E. P.
(1996)
in
Genetic Variants and Strains of the Laboratory Mouse (Lyon, M. F., Rastan, S., and Brown, S. D. M., eds), pp. 1446-1448, Oxford University Press, Oxford
-
Samaridis, J.,
and Colonna, M.
(1997)
Eur. J. Immunol.
27,
660-665[Medline]
[Order article via Infotrieve]
-
Cella, M.,
Dohring, C.,
Samaridis, J.,
Dessing, M.,
Brockhous, M.,
Lanzavecchia, A.,
and Colonna, M.
(1997)
J. Exp. Med.
185,
1743-1751[Abstract/Free Full Text]
-
Hayami, K.,
Fukuta, D.,
Nishikawa, Y.,
Yamashita, Y.,
Inui, M.,
Ohyama, Y.,
Hikida, M.,
Ohmori, H.,
and Takai, T.
(1997)
J. Biol. Chem.
272,
7320-7327[Abstract/Free Full Text]
-
Kubagawa, H.,
Burrows, P. D.,
and Cooper, M. D.
(1997)
Proc. Natl. Acad. Sci. U. S. A.
94,
5261-5266[Abstract/Free Full Text]
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