1 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine and Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, Missouri 63110; and 2 Environmental Health Sciences Division, National Institute for Environmental Studies, Tsukuba, Ibaraki 305, Japan
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ABSTRACT |
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Basement membranes have a critical
role in alveolar structure and function. Alveolar type II cells make
basement membrane constituents, including laminin, but relatively
little is known about the production of basement membrane proteins by
murine alveolar type II cells and a convenient system is not available
to study basement membrane production by murine alveolar type II cells. To facilitate study of basement membrane production, with particular focus on laminin chains, we examined transformed murine distal respiratory epithelial cells (MLE-15), which have many structural and
biochemical features of alveolar type II cells. We found that MLE-15
cells produce laminin-5, a trace amount of laminin-
3, laminins-
1 and -
1, type IV collagen, and perlecan. Transforming growth factor-
1 significantly induces expression of laminin-
1. When grown on a fibroblast-embedded collagen gel, MLE-15 cells assemble
a basement membrane-like layer containing laminin-
5. These findings
indicate that MLE-15 cells will be useful in modeling basement membrane
production and assembly by alveolar type II cells.
murine alveolar type II cells; transforming growth factor-; extracellular matrix
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INTRODUCTION |
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BASEMENT MEMBRANES ARE
THIN sheets of extracellular matrix that serve as a structural
support for cells. They also act as a selective barrier to various
solutes and affect cell properties, including proliferation,
differentiation, adhesion, and migration (for review, see Ref.
6). The major components of basement membranes are
laminins, type IV collagens, entactins (nidogens), and perlecan.
Basement membrane composition varies between tissues and even in the
same tissue at different stages of development. Laminins contribute to
the diversity of basement membranes. Laminins are a family of
heterotrimeric glycoproteins in which each member contains an -,
-, and
-chain. To date, five
-, three
-, and three
-chains forming 15 laminin isoforms have been described. Laminin-
3 is the most recently described (23) laminin
chain and is the only laminin chain that is not found in basement
membranes. In the current model, basement membrane assembly occurs via
linking of a type IV collagen network with a laminin network by
entactin (41).
In the lung, alveolar type I and alveolar type II cells rest on a continuous basement membrane; however, the composition of the basement membrane under both cell types is not the same. Differences exist in the location of basement membrane anionic sites beneath alveolar type I and type II cells (34). Subsets of alveolar type II cells have localized interruptions or discontinuities of the basement membrane where cytoplasmic processes extend and contact or closely approximate interstitial fibroblasts and extracellular matrix, whereas the basement membrane beneath type I cells does not (5).
The alveolar epithelial basement membrane is complex in composition and
undergoes changes during development. Recent studies (29,
30) highlight the variability of laminin -chain expression in
the lung. Laminin-
1 and -
2 are present in fetal lungs whereas laminin-
3, -
4, and -
5 are present in both fetal and adult
lungs (29). Laminin-
1 and -
5 are colocalized, but
laminin-
1 expression is restricted to the first trimester whereas
laminin-
5 expression is present at the end of the first trimester
and continues throughout adulthood (30). All three laminin
-chains and laminin-
1 and -
2 are found in both fetal and adult
lungs (10, 11, 37). Little is known about the effects of
injury and disease on the expression of laminin chains in the lung.
Alveolar type II cells in culture produce basement membrane components, including type IV collagen, laminin, perlecan, and entactin-1 (8, 15, 31, 36). Although alveolar type II cells can be isolated for study of production of basement membrane, obtaining them is labor intensive and time consuming. Additionally, harvest and culture of alveolar type II cells can be complicated by contamination with fibroblasts and differentiation into alveolar type I cells with time. To circumvent these problems, cell lines are widely used. The human alveolar epithelial cell line A549 and the rat alveolar epithelial cell line SV40-T2 have been used to study basement membrane production, but no mouse alveolar epithelial cell line has been identified for similar studies (15, 22, 31). With availability of knockout/transgenic mouse models, mice are utilized extensively in studies of cell and molecular biology and a mouse cell line would be valuable.
MLE-15 cells are an immortalized cell line obtained from lung tumors of
transgenic mice containing the simian virus 40 (SV40) large T antigen
under the transcriptional control of the human surfactant protein C
(SP-C) promoter (21). MLE-15 cells have many
characteristics of alveolar type II cells, including polygonal epithelial cell morphology, microvilli, cytoplasmic multivesicular bodies, multilamellar inclusion bodies, expression of SP-A, SP-B, and
SP-C, and secretion of phospholipids (39). MLE-15 cells have been used to examine distal respiratory epithelial cell functions such as Fas-dependent apoptosis, chemokine response to silica, transcription of thyroid transcription factor-1, and protein expression in response to hypertonic stress, but their ability to produce extracellular matrix has not been determined (1, 20, 40, 42). We have found that MLE-15 cells constitutively make several laminin chains, including laminin 5, as well as other components of
basement membrane, and assemble these components into a subepithelial basement membrane-like structure when grown in the presence of fibroblasts.
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MATERIALS AND METHODS |
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Cells and cell culture.
MLE-15 cells were obtained from Dr. Jeffrey Whitsett (University of
Cincinnati) and grown in HITES medium. HITES medium is RPMI 1640 (GIBCO-BRL, Gaithersburg, MD) supplemented with 2% fetal bovine serum
(GIBCO-BRL), 100 U/ml penicillin, 100 µg/ml streptomycin, 1%
insulin-transferrin-sodium selenite, 5 µg/ml transferrin, 10 nM
hydrocortisone, 10 nM -estradiol, 2 mM glutamine, and 2 mM HEPES.
For studies involving transforming growth factor-
1 (TGF-
1), confluent cultures were serum deprived for 24 h, and then TGF-
1 (R&D Systems, Minneapolis, MN) was added to a final concentration of 10 ng/ml for 24 h. Before fixation for immunohistochemistry and in
situ hybridization studies, cells were treated with 10 mg/ml brefeldin
A for 3 h to prevent secretion of extracellular proteins.
Culture of MLE-15 cells on collagen I gel and fibroblast-embedded
collagen I gel.
MLE-15 cells were cultured on fibroblast-embedded collagen I gel (Fgel)
to investigate the influences on basement membrane formation.
Fibroblasts were prepared from adult male Jcl/Fischer 344 rats (Japan
Cle, Tokyo, Japan), as described previously (15). First,
Fgel was prepared by mixing fibroblasts (1.8 × 105
cells) with 0.72 ml of 1 mg/ml neutralized type I collagen solution (acid-extracted type I collagen from bovine dermis; Koken, Tokyo, Japan) in DMEM, pH 7.2, casting the cell suspension on a cell culture
insert with a polyethylene terephthalate (PET) membrane (Becton
Dickinson Labware, Franklin Lakes, NJ) and allowing it to gel in a 5%
CO2 incubator for 1 h. After polymerization,
fibroblasts were supplied with DMEM containing 10% FCS, 0.2 mM
ascorbic acid 2-phosphate (Wako Pure Chemical Industries, Tokyo,
Japan), and 10 mM HEPES, pH 7.2, and cultured for 3 days. Next, MLE-15
cells (8 × 105 cells) grown in HITES medium were
seeded on the Fgel (MLE-15 Fgel) or on 0.72 ml of 1.5 mg/ml type I
collagen gel (MLE-15 gel) and cultured for 2 wk in an equal volume
mixture of DMEM and RPMI 1640 supplemented with 2% FCS, 100 mM
glutamine, 0.2 mM ascorbic acid 2-phosphate, and 10 mM HEPES, pH 7.2. MLE-15 cells were hyperproliferative in HITES medium and formed
multilayers in both MLE-15 Fgel and MLE-15 gel. Accordingly,
insulin-transferrin, sodium-selenite, hydrocortisone, and -estradiol
were excluded, and equal mixtures of fibroblast and MLE-15 cell medium
(without HITES) were used for MLE-15 gel and MLE-15 Fgel cultures.
Northern blot analysis.
Total RNA was isolated from MLE-15 cells with the ToTally RNA kit
(Ambion, Austin, TX). For Northern hybridization, 10 µg of total RNA
were denatured in 50% formamide, 1 M formaldehyde, and 50 ng/µl
ethidium bromide at 68°C for 5 min and then separated by
electrophoresis through a 1% agarose gel containing 1 M formaldehyde. RNA was passively transferred to charged Hybond N+ nylon
membrane (Amersham, Arlington Heights, IL), fixed by treatment with 50 mM NaOH for 5 min, and hybridized. cDNA probes were radiolabeled by
random priming with [32P]dCTP. mRNAs were detected using
probes made from nt 5494-5892 of laminin-1 cDNA
(35) and nt 658-990 of laminin-
5 cDNA
(28). For glyceraldehyde-3-phosphate dehydrogenase (GAPDH)
mRNA (pRGAPDH13), a 1.3-kb rat cDNA was used as previously described
(36). After hybridization, membranes were washed and
exposed to Kodak AR X-ray film at
70°C for 1-4 days with an
intensifying screen.
RT-PCR.
RNA (1 µg) was added to each RT reaction mixture including 20 pmol of
each primer. RT was performed using random hexamers by incubating at
25°C for 10 min, 42°C for 30 min, and 94°C for 5 min. PCR was
performed using specific mouse primers for laminin-1 to -
5 and
GAPDH as shown in Table 1. All primers
were obtained from Life Technologies (Grand Island, NY). All PCR
reactions were denatured at 94°C and extended at 72°C, and the
annealing temperatures and number of cycles varied as given in Table 1.
Primers for GAPDH were amplified in the same reaction mixture as
laminin
-chains but were added after 6-10 cycles, depending on
the laminin
-chain under investigation. PCR products were separated
in 1% agarose gels, transferred onto BrightStar-Plus nylon membranes
(Ambion, Austin, TX), and hybridized with 32P-labeled
specific oligonucleotide probes in standard saline citrate (SSC), 1%
SDS, 1× Denhardt's solution, and 50 µg/ml denatured salmon sperm
DNA at 42°C overnight. Membranes were washed in 6× SSC and 0.1% SDS
for 15 min at room temperature and then for 15 min at 52°C.
Quantification of PCR products was performed using the Bio-Rad
molecular imager system (GS-525; Hercules, CA) and expressed as the
ratio of laminin to GAPDH.
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In situ hybridization.
35S-labeled riboprobes were prepared from linearized cDNA
templates for in situ hybridization of MLE-15 cells as described
previously (25). MLE-15 cells were cultured on glass
slides until near confluence, serum deprived for 1 day, treated with
TGF- for 1 day, and fixed in methanol. The methods used for in situ
hybridization were as described in detail previously (36).
Negative controls hybridized with 35S-labeled sense probes
were performed simultaneously with the corresponding antisense samples.
Antibodies.
Recombinant domain G3-G4 of mouse laminin-5 (a gift from Dr.
Ulla Wewer, University of Copenhagen) (12) was expressed
in the PET vector system (Invitrogen, Carlsbad, CA) and used to
generate a rabbit polyclonal antibody. Rat monoclonal antibody to mouse laminin-
1 was a gift from Dr. Dale Abrahamson (University of Kansas). Rabbit polyclonal antibody to perlecan recognizing the core
protein of heparan sulfate proteoglycan was a gift from Dr. K. Kimata
(Aichi Medical University). Rabbit polyclonal antibody to mouse
type IV collagen, rat monoclonal antibody to mouse laminin-1 (MAb1975,
which recognizes the pepsin-digested fragment of laminin-1, P1), and
rat monoclonal antibody to mouse entactin (MAb1946, which recognizes a
recombinant region of the G1/link domain) used in immunofluorescence
studies were from Chemicon International (Temecula, CA). Rabbit
polyclonal antibody to type IV collagen used in immunoprecipitation was
from Collaborative Biomedical Products (Becton-Dickinson Labware, Bedford, MA). Rabbit polyclonal antibody to recombinant entactin was
raised as previously described (36).
Fluorescein-conjugated goat antibodies to rabbit IgG
F(ab')2 and rat IgG F(ab')2 were from Rockland
(Gilbertsville, PA).
Immunohistochemistry.
MLE 15 cells were cultured in two-well glass chambers (NUNC, Fisher
Scientific, PA), treated with TGF-1 as described in Cells and
cell culture, and fixed in methanol. Immunohistochemical
analysis of MLE-15 cells with polyclonal laminin-
5 and monoclonal
laminin-
1 antibodies was performed with the diaminobenzidine
Envision kit (DAKO, Carpinteria, CA) and the Vectastain Elite
avidin-biotin complex kit (Vector Laboratories, Burlingame, CA), respectively.
Tissue processing for transmission electron microscopy. The fixatives and dyes required for electron microscopy were obtained from TAAB (Berkshire, UK), except for Quetol resin, which was obtained from Nissin (Tokyo, Japan). Tissues were fixed with 2.5% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4) containing 0.2 M sucrose and 0.1% tannic acid and then postfixed with 1% osmium tetraoxide. The tissues were dehydrated through a series of graded ethanol, replaced with n-butyl glycidyl ether, and embedded in Quetol resin. After ultrathin sectioning, specimens were stained with lead citrate and uranyl acetate and examined with a JEOL JEM-2000FX microscope.
Metabolic labeling and immunoprecipitation.
Cells were seeded into six-well culture plates (Costar, Cambridge, MA)
at 2 × 106 cells/well with complete medium for 2 days. In studies involving TGF-1, the TGF-
1-treated wells were
serum deprived for 24 h before TGF-
1 treatment; control wells
were maintained in serum-free medium as described above during the same
time period. Cells were washed with methionine-free RPMI 40 medium,
after which fresh medium with all additives including FCS (dialyzed to
remove methionine) was added, followed by 50 µCi of
[35S]methionine (ICN Biomedical, Costa Mesa, CA).
Cultures were returned to a 5% CO2 incubator for 24 h, after which the conditioned medium was collected. To obtain secreted
matrices, we treated cells as described previously by Rannels et al.
(32). Briefly, cells were exposed to 1 ml of 0.25 M
NH4OH, 1 mM phenylmethylsulfonyl fluoride (PMSF), and 1 mM
EDTA, and wells were washed with PBS-EDTA (1 mM). DNA and nuclear
debris were removed by treatment with 1 ml of 50 mM Tris, pH 8.0, 1 M
NaCl, 1 mM PMSF, and 1 mM EDTA for 15 min at 4°C, and wells were
washed with PBS-EDTA (1 mM). STRIPA (500 µl) (150 mM NaCl, 5 mM EDTA,
5 mM urea, 1 mM PMSF, 1% deoxycholate, 1% SDS, 1% Triton X-100, 1%
Nonidet P-40, and 50 mM Tris, pH 8.0) was added, and wells were scraped
and the contents collected. Medium and secreted matrices were stored at
80°C.
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RESULTS |
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Expression of laminin -chain mRNAs.
RT-PCR for laminin
1- to
5-chain mRNAs in MLE-15 cells revealed
high expression of laminin-
5 and slight expression of laminin-
3 but virtually no expression of laminin-
1, -
2, and -
4 at
baseline (Fig. 1). Northern blot analysis
confirmed the expression of laminin-
5 mRNA in MLE-15 cells (Fig.
2A) with mouse placenta as a
positive control. Likewise, in situ hybridization (Fig. 2B)
and immunohistochemical staining (Fig. 2, C and
D) for laminin-
5 revealed strong expression and
production in MLE-15 cells. Metabolic labeling and immunoprecipitation of MLE-15-conditioned medium showed production and secretion of laminin
5-chain as well as laminin
1/
1-chains (Fig.
3).
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Effect of TGF-1 on laminin
-chain expression.
Because TGF-
1 promotes the production of several basement membrane
proteins (14, 18, 24), semiquantitative RT-PCR for laminin-
1 to -
5 was performed on MLE-15 cell mRNA after the addition of TGF-
1. To lower the basal constitutive expression of
laminin-
5, we serum deprived the cells for 24 h before the addition of TGF-
1. Figure 4 shows that
laminin-
1 production was induced eightfold with TGF-
1, an effect
that was confirmed by in situ hybridization (Fig.
5, A and B) and
immunohistochemistry (Fig. 5, D and E).
In comparison, TGF-
1 had only a minimal effect on laminin-
5 mRNA
expression as was the case for laminin-
2, -
3, and -
4 mRNA
(data not shown). The optimum exposure time for the maximal effect of
TGF-
1 on laminin
-chain expression was determined to be
18-24 h (data not shown).
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Basement membrane protein production.
In addition to production of laminin 5- and
1/
1-chains,
metabolic labeling and immunoprecipitation of MLE-15 cell-conditioned medium also demonstrated production of type IV collagen and perlecan but not entactin (Fig. 6).
Immunoprecipitation of the insoluble material deposited under MLE-15
cells was negative for laminin-
5 or -
1/
1, type IV collagen,
and entactin (data not shown), indicating that although MLE-15 cells
make some components of basement membrane, they do not assemble a
basement membrane when grown on plastic.
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Basement membrane formation.
In previous studies, basement membrane formation was observed
(15) when rat type II epithelial cells (SV40-T2) were
grown on Fgel but not on a collagen I gel. Because MLE-15 cells did not
form a basement membrane when cultured on plastic, we examined basement
membrane formation when MLE-15 cells were grown synchronously for 2 wk
on collagen gels (MLE-15 gel) and Fgel (MLE-15 Fgel) by
immunofluorescence and transmission electron microscopy. Similar to rat
SV40-T2 cells, MLE-15 cells exhibited a cuboidal morphology on collagen
gel (MLE-15 gel) and a squamous appearance when grown on
fibroblast-embedded collagen gel (MLE-15 Fgel) (15). In
MLE-15 gel, only faint, spotty immunofluorescence for laminin, type IV collagen, and perlecan was present (Fig.
7, A, C, and
E). However, in MLE-15 Fgel, distinct, partially continuous
linear deposits of fluorescence for laminin, type IV collagen, and
perlecan were seen at the interface between MLE-15 cells and Fgel (Fig.
7, B, D, and F). Because MLE-15 cells
do not produce entactin, we did not detect entactin when MLE-15 cells
were grown on a collagen gel without fibroblasts (Fig. 7G).
However, integration of entactin was observed in the MLE-15 Fgel
culture when detected with the polyclonal antibody against mouse
entactin (Fig. 7H) but not with the rat monoclonal antibody
(MAb1946) against mouse entactin (data not shown). This suggests that
the integrated entactin was derived from the embedded rat
fibroblasts since the polyclonal antibody is crossreactive with rat
entactin (36).
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DISCUSSION |
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As a surrogate for normal murine type II alveolar epithelial cells, MLE-15 cells have been used to study surfactant and phospholipid production (19), chemokine expression (1, 2), and induction of water channel proteins (20). MLE-15 cells have been transfected with various genes (7, 40) and infected with retrovirus-mediated HSV-tk gene (42). However, the production of basement membrane proteins by MLE-15 cells has not been investigated, although it is well known that alveolar epithelial cells make these proteins. Considering the current interest in murine cell and molecular biology, the availability of a murine respiratory epithelial cell that produces basement membrane proteins could prove quite useful.
Different isoforms of collagen, proteoglycans, and laminins give
basement membranes heterogeneity and functional specificity. In this
study, we concentrated on laminins. Although 15 laminins have been
described, the chain with the most variability in the laminin trimer is
the -chain. In the normal lung, laminin-
1 and -
2 are seen only
in fetal development while laminin-
3, -
4, and -
5 are seen in
both fetal and adult stages (29, 30). Mesenchymal cells
produce laminin-
2 and -
4, epithelial cells produce laminin-
3
and -
5, and both epithelial and mesenchymal cells produce
laminin-
1 (13). The MLE-15 cell line is an immortalized cell line derived from alveolar type II epithelial cells of lung tumors
generated in adult mice. Accordingly, production of laminin-
3 and
-
5 was expected, but not production of mesenchymal
laminin-
2 and -
4. Consistent with this, we found that MLE-15
cells express laminin-
5 and -
3 but do not express
laminin-
2 and -
4. Laminin-
5 expression was most abundant
with lesser expression of laminin-
3. Because production of
laminin-
1 is normally restricted to early fetal lungs, we did
not expect to find laminin-
1 production and this was the result with
MLE-15 cells at baseline.
TGF- increases production of many extracellular matrix proteins,
including the basement membrane proteins type IV collagen (18), laminin-
2 (24), perlecan, and
entactin (14). Virtually every mammalian cell produces and
has receptors for TGF-
, and TGF-
levels are increased in
inflammation and fibrosis (4). We found that MLE-15 cells
exposed to TGF-
1 increase expression and production of laminin
-chains, similar to human and rat type II cell lines
(14). A new observation is that TGF-
1 induces production of laminin-
1. Laminin-
1 is the most extensively
studied laminin
-chain and is present in the lung only during
early fetal development (29, 38). It is somewhat
surprising that an adult-derived cell line could be induced to make
laminin-
1. This may occur in MLE-15 cells because it is a
transformed cell line. Alternatively, because TGF-
is increased in
many injury states and TGF-
leads to increased production of
extracellular matrix, it is possible that adult alveolar
epithelial cells might produce some "fetal proteins" as part of the
response to injury.
The substrata on which alveolar type II cells are grown affects their
phenotype and function (for review, see Ref. 9). With
complex extracellular matrices such as human amniotic membrane, type II
cell morphology is cuboidal when grown on the basement membrane side
and attenuated when grown on the stromal side (27). When
cultured on individual matrix substrates such as laminin-1 or type I
collagen, type II cell morphology is cuboidal, whereas with fibronectin
and type IV collagen, the morphology is attenuated. We examined laminin
1- and
5-chain expression by MLE-15 cells grown on plastic alone
and on different matrix substrates such as mouse laminin-1 derived from
the Engelbreth-Holm-Swarm (EHS) tumor, type IV collagen, and
pepsin-digested laminin-10/11 (formed by the trimers
5/
1/
1 and
5/
2/
1, respectively). We did not find differences in cell
morphology or expression of laminin
1- or
5-chains so MLE-15
cells do not appear to be as responsive to the extracellular matrix as
primary type II cells.
We found that MLE-15 cells produce laminin, type IV collagen, and perlecan, but they do not independently assemble a basement membrane. MLE-15 cells do not produce entactin, the molecule that links laminin with type IV collagen. However, in the presence of fibroblasts, a basement membrane-like material containing entactin is deposited underneath the MLE-15 cells. Because lung mesenchymal cells are the main source of lung entactin, the entactin seen was probably produced by fibroblasts and recruited to the basement membrane by the MLE-15 cell. Alternatively, fibroblasts may secrete a factor(s) that induces entactin expression by MLE-15 cells. However, this explanation is unlikely since the rat monoclonal antibody to mouse entactin failed to detect deposits of entactin even in the presence of fibroblasts. Rat transformed alveolar type II cells (SV40-T2) produce laminin, type IV collagen, perlecan, and a small amount of entactin. However, like MLE-15 cells, they are unable to form a basement membrane unless grown in the presence of fibroblasts or Matrigel (an extracellular matrix derived from EHS tumor with basement membrane that contains laminin-1, growth hormones, and cytokines) (15, 16) even though they make entactin. These data support the concept that basement membrane assembly requires more than the presence of the components of basement membrane but rather interaction between epithelial cells and fibroblasts.
In summary, previous studies (1, 2, 7, 19, 20, 40, 42)
have found MLE-15 cells useful as a surrogate to investigate different
aspects of alveolar type II cell function. The present study
extends these earlier observations by revealing that MLE-15 cells
spontaneously produce basement membrane proteins, specifically laminins
containing 5- and
3-chains, type IV collagen, and perlecan, and
that MLE-15 cells can interact with fibroblasts to form a subepithelial
basement membrane-like structure. Accordingly, MLE-15 cells may be
useful for studies of basement membrane production, assembly, and
function by murine alveolar type II cells.
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ACKNOWLEDGEMENTS |
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We thank Dr. Jeffrey Whitsett for providing MLE-15 cells and G. L. Griffin and M. S. Mudd for technical assistance.
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FOOTNOTES |
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This work was supported by National Heart, Lung, and Blood Institute Grant HL-29594; the Alan A. and Edith L. Wolff Charitable Trust; and a Research Fellowship from the American Lung Association (N. M. Nguyen).
For questions and comments pertaining to the microscopy studies, contact K. Mochitate (E-mail: mochitat{at}nies.go.jp).
Address for reprint requests and other correspondence: R. M. Senior, Dept. of Medicine, Barnes-Jewish Hospital, North Campus, 216 South Kingshighway, St. Louis, MO 63110 (E-mail: seniorr{at}msnotes.wustl.edu).
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.
First published December 14, 2001;10.1152/ajplung.00379.2001
Received 24 September 2001; accepted in final form 1 December 2001.
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