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 Previous Article | Table of Contents | Next Article 
Blood, Vol. 94 No. 7 (October 1), 1999:
pp. 2390-2395
Matrix Metalloproteinase-9 Production, a Newly Identified Function of
Mast Cell Progenitors, Is Downregulated by c-kit Receptor
Activation
By
Akane Tanaka,
Katsuhiko Arai,
Yukihiko Kitamura, and
Hiroshi Matsuda
From the Departments of Veterinary Clinic and Tissue Physiology,
Faculty of Agriculture, Tokyo University of Agriculture and Technology,
Tokyo, Japan; and the Department of Pathology, Osaka University School
of Medicine, Osaka, Japan.
 |
ABSTRACT |
Mast cell precursors invade from the peripheral blood into local
tissues where they differentiate to their mature phenotypes. However,
the mechanism of this migration process has been unclear. We clearly
demonstrated here the production and release of matrix metalloproteinase-9 (MMP-9), a matrix-degrading enzyme necessary for
leukocyte transmigration, by interleukin-3-dependent mouse mast cell
progenitors: bone marrow-derived cultured mast cells and IC-2 mast
cells. Because several interleukin-3-independent mast cell lines with
active mutations in the c-kit gene did not release MMP-9, the
possible involvement of c-kit receptor activation in
downregulation of MMP-9 production was predicted. c-kit
receptor activation by stem cell factor led to a significant decrease
in MMP-9 production of cultured mast cells and IC-2 mast cells
transfected with the c-kit gene. Thus, the present results
suggest that mast cell precursors are able to produce MMP-9, which may
be essential for mast cell migration into tissues, and that stem cell
factor may downregulate the MMP-9 production, resulting in engagement of mast cells to matrix components.
© 1999 by The American Society of Hematology.
| |
INTRODUCTION |
MAST CELL PROGENITORS, which originate
from pluripotential hematopoietic stem cells, circulate through the
bloodstream and invade into distinct tissues where they differentiate
into two well-characterized types of mature mast cells.1-4
Proliferation and differentiation of mast cells are regulated by
soluble factors locally produced by at least Th2 T cells and
fibroblasts in rodents and humans.5,6 Murine bone marrow
derived-cultured mast cells (BMCMCs), which develop in the presence of
T-cell-derived growth factors, including interleukin-3
(IL-3),7 are able to differentiate into mature mast cells
through the peripheral blood at various tissues of mast cell-deficient
W/Wv mice.8 On the other hand, stem
cell factor (SCF), a specific ligand for the c-kit receptor
with tyrosine kinase activity on mast cell precursors,9 is
expressed on fibroblasts.10 This factor is not only able to
support survival and proliferation of BMCMCs and peritoneal mast cells,
but also induces a phenotypic change from BMCMCs to connective
tissue-type mast cells.11,12 Much is known regarding
how allergic and nonallergic stimuli lead to rapid
activation with release of chemical mediators of mast cells, including
inflammatory cytokines, resulting in proliferation and differentiation
of their precursors at the affected sites. However, it is unclear how
the precursors invade from the peripheral blood into local tissues or
how the precursors degrade extracellular matrix in the process of their
proliferation and differentiation.
Previous studies have demonstrated that the production of
matrix-degrading enzymes, such as matrix metalloproteinase-9 (MMP-9), is essential for leukocyte extravasation and recruitment to the affected sites.13,14 MMP-9, which belongs to a large family of Zn2+-requiring enzymes, hydrolyzes basement membrane
collagen types IV and V, anchoring collagen type VII, denatured
collagens, fibronectin, and elastin.15,16 MMP-9 is secreted
as a latent form (proMMP-9) and directly or indirectly activated by
MMP-3 released from fibroblasts,17 chymase released from
mast cells,18 and a plasminogen activator released from
microvascular endothelial cells.19 Therefore, there is a
possibility that mast cell precursors produce MMP-9 by themselves to
degrade extracellular matrix in the process of their migration in local
tissues. In the present study, we demonstrated that BMCMCs and IC-2
mast cell progenitors synthesized and released MMP-9, which was
downregulated by SCF.
| |
MATERIALS AND METHODS |
Cells and reagents.
P-815 mouse mastocytoma, RBL-2H3 rat mast cell leukemia, and HMC-1
human mast cell leukemia cell lines were cultured in  -minimum essential medium (-MEM; GIBCO RBL, Grand Island, NY)
containing 10% fetal bovine serum (FBS; Filtron, Brooklyn, Australia),
100 U/mL penicillin, and 100 µg/mL streptomycin. An IC-2 mouse mast cell progenitor line was maintained in -MEM containing 10% FBS and
100 U/mL of recombinant mouse IL-3 (Kirin Brewery, Tokyo, Japan). The
wild-type c-kit gene or V814 mutant gene was introduced into
IC-2 cells by the retroviral vector, and the infected cells were
selected in G418-containing growth medium as described
previously.20 Control IC-2 cells were transfected with the
vector alone and selected in the same way. BMCMCs were obtained from
bone marrow cells of WBB6F1-+/+ mice in -MEM containing
10% FBS and 10% pokeweed mitogen-stimulated spleen cell-conditioned
medium according to the method described previously.21
Recombinant rat SCF (rSCF) was a gift from Amgen Inc (Thousand Oaks,
CA). Rabbit anti-c-kit polyclonal antibody and goat
anti-MMP-9 polyclonal antibody were obtained from Santa Cruz
Biotechnology Inc (Santa Cruz, CA). Peroxidase-conjugated mouse
antiphosphotyrosine monoclonal antibody (MoAb; clone 4G10) and
peroxidase-conjugated mouse antigoat IgG antibody were from Upstate
Biotechnology Inc (Lake Placid, NY) and Jackson ImmunoResearch Laboratories Inc (West Grove, PA), respectively. Metal ion chelators, EDTA, and 1,10-phenanthroline were purchased from Kanto Chemical Co,
Inc (Tokyo, Japan). Serine protease inhibitors,
4-(2-aminoethyl)-benzenesulfonyl fluoride hydrochloride (ABSF) and
aprotinin, were from Wako Pure Chemicals Industries (Osaka, Japan) and
Boehringer Mannheim (Mannheim, Germany), respectively.
Gelatin zymography.
Cells (5 × 106/mL) were incubated in serum-free
medium for 72 hours and culture supernatants were harvested. The
supernatants were electrophoresed using 10% sodium dodecyl sulfate
(SDS)-polyacrylamide gel with copolymerized 1 mg/mL
gelatin (TEFCO, Tokyo, Japan) under nonreducing conditions. After
washing gels in 2.5% Triton X-100 for 30 minutes twice to remove SDS,
gelatinolytic enzymes were activated by incubating gels in 50 mmol/L
Tris-HCl buffer containing 200 mmol/L NaCl and 10 mmol/L
CaCl2 (pH 7.5) for 24 hours at 37°C. Gels were stained
with 0.2% Coomassie Brilliant blue for 60 minutes and destained in
10% acetic acid/25% methanol. Gelatinolytic activity was identified
as a clear band on a blue background. Images were analyzed by Gel Print
2000i/VGA and Basic Quantifier (Genomic Solutions, Tokyo, Japan).
To define that gelatinolytic enzymes belong to MMPs, gels were
incubated in buffer containing metal chelators (20 mmol/L EDTA or 2 mmol/L 1,10-phenanthroline) after electrophoresis and after SDS
removal. For further determination of MMPs, collected cultured media
were mixed with either of the serine protease inhibitors, 1 mmol/L ABSF
or 30 nmol/L aprotinin, before application onto gelatin zymography. In
each experiment, gels were stained and destained as described above.
Northern blot analysis.
BMCMCs and IC-2 transfectants were washed twice and incubated with or
without 50 ng/mL 10-O-tetradecanoylphorbol-13-acetate (TPA;
Sigma, St Louis, MO) or various concentrations of rSCF in -MEM
containing 1% bovine serum albumin (BSA; Sigma). Six hours later, mRNA
was isolated from 5 × 106 cells per each condition
using a QuickPrep mRNA purification kit (Pharmacia, Uppsala, Sweden).
mRNA obtained from each sample was electrophoresed on
formaldehyde-agarose (1.2%) gels, transferred onto nylon membrane
(Boehringer Mannheim), and UV cross-linked. After prehybridization for
60 minutes at 42°C, the samples were hybridized for 16 hours at
60°C with digoxigenin-labeled single-strand cDNA probes specific
for mouse MMP-9 and  -actin (Nippon Flower Milles, Tokyo, Japan),
5'-GGACACATAGTGGGAGGTGCTGTCGGCTGT-3' (988 through 1018) and
5'-GGCTGGGGTGTTGAAGGTCTCAAACATGATCTGGGTCATC-3' (394 through
434), respectively. Hybridized filters were washed, blocked for 60 minutes in blocking buffer (100 mmol/L maleic acid, 3 mol/L NaCl, 0.3%
Tween 20, and 0.5% blocking reagent, pH 8.0), and incubated with
alkaline phosphatase-conjugated polyclonal sheep antidigoxigenin Fab
fragments (Boehringer Mannheim) diluted to 75 mU/mL (1:15,000) in
blocking buffer for 30 minutes. After washing 3 times, the membrane was
immersed in detection buffer (100 mmol/L Tris-HCl, 100 mmol/L NaCl, 50 mmol/L MgCl2, and 0.25 mmol/L CSPD [Boehringer Mannheim],
pH 9.5) for 30 minutes, repacked in a hybridization bag without buffer,
and incubated for 30 minutes at 37°C to enhance the luminescent
reaction. The signals were exposed to x-ray film at room temperature,
and the images were digitalized as described.
Immunoprecipitation and Western blotting.
Protein A-Sepharose CL-4B (Pharmacia) was equilibrated in lysis buffer
(20 mmol/L Tris-HCl, 137 mmol/L NaCl, 10% glycerol, 1% NP-40, and
protease and phosphatase inhibitors, pH 8.0) and adjusted to 50%
suspension. To make beads-antibody complexes, 0.5 µg of
anti-c-kit antibody and 100 µL of 50% Protein A-Sepharose suspension were mixed in 500 µL of lysis buffer for 4 hours at 4°C with gentle rotation. The complexes were washed twice with lysis buffer and kept on ice until use. BMCMCs and IC-2WT
cells (1 × 107 cells per each condition) were
incubated in serum-free -MEM containing 1% BSA for 4 hours at
37°C to reduce basic levels of phosphorylation. After the treatment
with or without 100 ng/mL rSCF for 15 minutes, cells were collected and
lysed in 800 µL of lysis buffer, frozen and thawed 3 times, and
centrifuged for 10 minutes at 15,000 rpm. Supernatants were harvested,
applied onto the beads-antibody complexes, and incubated at 4°C
overnight with gentle rotation. Immunoprecipitates were washed twice
with lysis buffer, suspended in 50 µL of 2× SDS sample buffer
containing 12% urea, and boiled for 7 minutes. Proteins were separated
by 6% SDS-polyacrylamide gel electrophoresis (SDS-PAGE),
transferred to Immobilon-P membrane (Millipore, Bedford, MA), and
immunoblotted with peroxidase-conjugated antiphosphotyrosine MoAb
(Upstate Biotechnology). Immune complexes were visualized using an ECL
system (Amersham, Arlington Heights, IL).
Immunocytochemistry.
Cytospin preparations of mast cell progenitors were fixed in 4%
paraformaldehyde for 15 minutes at 4°C and then washed in phosphate-buffered saline (PBS). Endogenous peroxidase was invalidated by immersing samples in 3% H2O2 containing PBS
for 5 minutes at room temperature. Nonspecific reaction was blocked by
incubating slides with 10% filtrated mouse serum in PBS for 30 minutes
at room temperature. Goat anti-MMP-9 polyclonal antibody diluted in
0.05% Tween 20 containing PBS was applied onto the samples and
incubated at 4°C overnight. Filtrated normal goat serum was used as
a control. After washing, the preparations were incubated with
peroxidase-conjugated mouse antigoat IgG antibody in 0.05% Tween 20 containing PBS for 60 minutes. The reaction products were visualized
with diaminobenzidine as a substrate, and then the cells were
counterstained with Mayer's hematoxylin.
| |
RESULTS |
MMP-9 production of mast cell progenitors.
BMCMCs and several mast cell lines were incubated in serum-free -MEM
for 72 hours, and gelatinolytic activities in collected culture media
were examined by gelatin zymography. The culture media of
IL-3-dependent mast cell progenitors, BMCMCs, and IC-2 mouse mast
cells possessed gelatin-degrading activities corresponding to proMMP-9
and its active form and to proMMP-9 alone, respectively, whereas little
or no gelatinolytic activity was detected in the culture media of P-815
mouse mastocytoma cells, RBL-2H3 rat mast cell leukemia cells, and
HMC-1 human mast cell leukemia cells (Fig
1A). Because the synthesis of MMP-9 is stimulated with
phorbolesters,22 BMCMCs and IC-2 cells were incubated with
50 ng/mL TPA for 72 hours; the more potent gelatinolytic activities
corresponding to proMMP-9 and its active form were noted (Fig 1B). The
proteolytic bands disappeared when the gels were incubated in buffer
containing EDTA or 1,10-phenanthroline (chelators of Ca2+
and Zn2+, respectively) after loading the samples. Because
serine proteases possess a weak gelatinolytic activity, serine protease
inhibitors, ABSF and aprotinin, were added to samples before
electrophoresis. The treatment with the inhibitors showed no effect on
the positive activity, indicating that this gelatinolytic activity was
an MMP23 (Fig 1C). Northern blot analysis using
digoxigenin-labeled oligonucleotide cDNA probes specific for mouse
MMP-9 clearly demonstrated the expression of MMP-9 mRNA (2.4 kb), which
was increased in both of the cells stimulated with TPA (Fig 1D).
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| Fig 1.
MMP-9 production from mast cell progenitors.
Gelatinolytic activities comparable to proMMP-9 and MMP-9 are observed
in IL-3-dependent BMCMCs or IC-2 cells, but not in P-815, RBL-2H3, and
HMC-1 cells (A). The addition of 50 ng/mL TPA enhances the
gelatinolytic activities released from BMCMCs and IC-2 cells (B). The
gelatinolytic activity released from IC-2 cells disappears in gels
incubated in buffer containing 20 mmol/L EDTA or 2 mmol/L
1,10-phenanthroline. Enzymatic activity is not affected by incubation
with serine protease inhibitors, 1 mmol/L ABSF, or 30 nmol/L aprotinin,
respectively (C). Expression of MMP-9 mRNA is observed in BMCMCs and
IC-2 cells; and treatment with 50 ng/mL TPA for 6 hours significantly
increases the expression of MMP-9 mRNA of both the cells (D).
|
|
Deficiency in MMP-9 production of mast cell lines with active
c-kit tyrosine kinase.
SCF, which is one of fibroblast-derived growth factors, regulates
survival, differentiation, and functions of mast cells through the
c-kit receptor.12,24 P-815, RBL-2H3, and HMC-1
cells have point mutations in the c-kit proto-oncogene, leading
to constitutive activation of the c-kit tyrosine kinase even
without ligation of SCF to the receptor.25-27 Because no
MMP-9 secretion was detected in culture media obtained from these cell
lines (Fig 1A), there is a possibility that c-kit
autophosphorylation may lead to suppression in MMP-9 production of mast
cell progenitors. To confirm active c-kit receptors in these
cell lines, Western blot analysis with antiphosphotyrosine MoAb was
performed on immunoprecipitated products with anti-c-kit
receptor antibody. As shown in Fig 2, a
marked positive response showing autophosphorylation of the
c-kit receptor was detected in P-815, RBL-2H3, and HMC-1 cells,
but not in IC-2 cells.
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| Fig 2.
Immunoblot analysis of tyrosine phosphorylation of the
c-kit receptor. Marked positive reaction is observed in P-815,
RBL-2H3, and HMC-1 cells, but not in the original IC-2 cells.
|
|
MMP-9 release of IC-2 cells denuded by transfection with mutant
c-kit gene.
To clarify whether activation of the c-kit receptor
downregulates MMP-9 production of mast cells, we transferred a
wild-type of the c-kit gene or c-kit gene with one
point mutation to IC-2 cells that express no c-kit receptors on
the surface28 and assessed MMP-9 activity in culture media
of these transfectants by gelatin zymography. In HMC-1 cells, the
c-kit gene was found to include a mutant allele with point
mutations, resulting in amino acid substitutions of Gly-560 for Val and
Asp-816 for Val.20 Because the activating mutation
corresponding to Asp codon of HMC-1 cells was also found in both P-815
cells (Asp-814 to Tyr) and RBL-2H3 cells (Asp-817 to
Tyr),25,26 we introduced c-kit V814 mutant (Asp-814
to Val) into IC-2 cells using the retroviral vector as previously
described.20 Wild-type c-kit gene transfectants
(IC-2WT) exhibited activation of c-kit receptor
tyrosine kinase dependent on rSCF as well as BMCMCs, whereas mutant
gene transfected cells (IC-2V814) expressed active
c-kit receptors even without an addition of rSCF
(Fig 3A). Although IC-2WT cells
were capable of releasing proMMP-9 comparable to original IC-2 cells,
such a gelatinolytic activity was undetectable in the culture medium of
IC-2V814 cells (Fig 3B). These results clearly demonstrated
the negative correlation between c-kit receptor activation and
MMP-9 secretion of IC-2 cells.
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| Fig 3.
Detection of c-kit receptor activation and MMP-9
secretion of IC-2 transfectants and BMCMCs. SCF-dependent activation of
the c-kit receptor was observed in BMCMCs and
IC-2WT cells, whereas SCF-independent phosphorylation was
detected in a constitutively active c-kit transfectant
(IC-2V814; A). ProMMP-9 activity is marked in control
IC-2VECTOR cells and IC-2WT cells as well as
the original IC-2 cells, but not in IC-2V814 cells even
when stimulated with TPA (B).
|
|
MMP-9 production of mast cell progenitors suppressed by rSCF.
To further investigate the suppressive effect of SCF on MMP-9
production from mast cell progenitors, BMCMCs and IC-2WT
cells were incubated with various concentrations of rSCF in -MEM containing 1% BSA for 72 hours. The addition of rSCF to BMCMCs resulted in a significant decrease of the proMMP-9 activity in a
dose-dependent manner (Fig 4A); the
inhibitory effect of rSCF on release of proMMP-9 was observed in
IC-2WT cells as well (Fig 4B). Northern blot analysis
showed that the addition of rSCF led to the diminished expression of
MMP-9 mRNA in BMCMCs and IC-2WT cells, but not in
IC-2VECTOR cells (Fig 4C).
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| Fig 4.
SCF-induced downregulation of MMP-9 production of mast
cell progenitors. BMCMCs and IC-2WT cells were incubated
with or without various concentrations of rSCF for 72 hours at
37°C. Dose-dependent inhibitory effect on release of proMMP-9 and
MMP-9 is obvious (A and B). mRNA was purified from mast cell
progenitors stimulated with or without 100 ng/mL rSCF for 6 hours.
MMP-9 mRNA expression of IC-2VECTOR cells is stable despite
the addition of rSCF, but MMP-9 mRNA expression of both BMCMCs and
IC-2WT cells is markedly reduced by the treatment with rSCF
(C).
|
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Next, we conducted immunocytochemical experiments to examine whether
SCF downregulated MMP-9 synthesis of mast cell progenitors. BMCMCs were
incubated with 100 ng/mL rSCF for 72 hours. Every 24 hours, cells were
collected and treated with anti-MMP-9 antibody. BMCMCs incubated with
rIL-3 in the absence of rSCF were strongly stained with anti-MMP-9
antibody in their cytoplasm (Fig 5a). On
the other hand, BMCMCs exposed with rSCF alone showed little or no
reaction for MMP-9 (Fig 5b). The specificity of anti-MMP-9 antibody
against mouse MMP-9 was confirmed by Western blotting (data not shown).
To examine an intracellular gelatinolytic activity, BMCMCs were
collected and lysed; MMP-9 activities were diminished depending on the
incubation period with rSCF (data not shown). Thus, we concluded that
SCF was able to suppress MMP-9 production of mast cell progenitors.
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| Fig 5.
Immunocytochemical staining for MMP-9. BMCMCs incubated
with rIL-3 (a) or with 100 ng/mL rSCF (b) for 72 hours were fixed in
4% paraformaldehyde and treated with anti-MMP-9 antibody. BMCMCs
incubated with rSCF show a weak reaction or no reaction for MMP-9.
|
|
| |
DISCUSSION |
Much is known regarding how MMP-9 produced by inflammatory
cells is crucially involved in their migration from peripheral blood
vessels into affected tissues.13,14 For mast cell
progenitors, MMP-9, which is able to degenerate basement membrane
collagen types IV and V, anchoring collagen type VII, and other matrix components, may be essential to invade from blood vessels into local
connective tissues where they complete their differentiation. In the
present study, we clearly demonstrated that the IL-3-dependent mouse
mast cell progenitors produced and released proMMP-9 spontaneously. Because a plasminogen activator released from vascular endothelial cells is able to indirectly activate proMMP-9,19 proMMP-9
produced by mast cell precursors might be transformed to its active
form under the influence of the activator, crossing the endothelial wall.
In the process of maturation, mast cells are considered to migrate
toward SCF expressed on fibroblasts and engaged to matrix components of
local tissues eventually. In fact, SCF is able not only to function as
a chemoattractant for BMCMCs and IL-3-dependent mouse mast cell
lines,29 but also to induce their adhesion to fibronectin30 through 51 integrin.31
Because no MMP-9 activity was detectable in the culture media obtained
from the cell lines with active mutations in the c-kit gene, we
attempted to determine the possible involvement of the c-kit
receptor activation on MMP-9 production of mast cell progenitors.
c-kit receptor tyrosine kinase of P-815, RBL-2H3, and HMC-1
cells was demonstrated to be activated spontaneously as
described.25-27 Moreover, transfection of c-kit V814 mutant gene to IC-2 cells resulted in significant suppression of
MMP-9 production, indicating that c-kit receptor activation and
MMP-9 production may be reciprocally regulated in mast cell progenitors.
Allergic and nonallergic stimuli lead to rapid activation with release
of chemical mediators, including inflammatory cytokines, resulting in
proliferation and differentiation of their fixed precursors at the
affected site.32 Recently, the presence of committed
precursors of mast cells in the peripheral blood has been
reported,3,4 but it is unknown how the precursors invade from the peripheral blood into tissues or how the precursors fixed in
local tissues degrade extracellular matrix in the process of their
proliferation and differentiation. The present study strongly suggests
the novel role of MMP-9 produced by mast cell precursors in their
tissue invasion and the downregulation of mast cell motility mediated
by SCF due to decreasing MMP-9 production. Further investigation must
take place to elucidate the mechanisms of these responses in detail,
but this discovery may bring a new insight into the mechanism of mast
cell differentiation and distribution in local tissues.
| |
ACKNOWLEDGMENT |
The authors thank Dr Stephen J. Galli (Department of Pathology, Harvard
Medical School, Boston, MA) for valuable discussions. We also thank
Amgen Inc for providing rat rSCF and Kirin Brewery Co for supplying
mouse rIL-3.
| |
FOOTNOTES |
Submitted April 16, 1999; accepted June 2, 1999.
Supported by grants from the Ministry of Education, Science, Sports,
and Culture, Japan; from the Pioneering Research Project in
Biotechnology, the Ministry of Agriculture, Forestry, and Fisheries, Japan.
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Address reprint requests to Hiroshi Matsuda, DVM, PhD, Department of
Veterinary Clinic, Faculty of Agriculture, Tokyo University of
Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan.
| |
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