 3, 4, and 5 Chains by Alveolar
Epithelial Cells and Fibroblasts
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Abstract |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminins are principal components of basement membranes. Eleven laminin isoforms are known, each a
heterotrimer composed of polypeptide chains designated 
, 
, and 
. Five chains have been identified to
date: 1, 2, 3, 4, and 5. Recent studies of fetal and adult mouse lung show prominence of 3, 4, and
5 in alveolar tissue, and point to differences in the cellular expression of these chains in the developing
alveolus. We examined isolated rat alveolar type II cells and lung fibroblasts for expression of laminins 3,
4, and 5. We found that laminin 3 was expressed only by alveolar epithelial cells, that laminin 4 was
expressed only by lung fibroblasts, and that laminin 5 was expressed primarily by alveolar epithelial
cells. Metabolic labeling and immunoprecipitation confirmed the production of laminin 4 by fibroblasts
and laminin 5 by alveolar epithelial cells in culture. These studies indicate that different alveolar cell
types contribute different laminin chains to the laminin isoforms in alveolar basement membranes. Immunohistochemistry showed colocalization of these laminin chains with the laminin 1, 2, and 1
chains, indicating the likelihood that laminins 6 to 11 are present in alveolar basement membranes.
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Introduction |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminins are a family of basement membrane-associated
glycoproteins that interact with other basement membrane
components, attach cells to basement membranes, and affect cell migration and phenotype (1). Each member of the
laminin family is a heterotrimer consisting of , , and polypeptide chains linked by disulfide bonds. To date, five
chains, three chains, and two chains, and a total of 11 laminin isoforms have been identified (2). The , , and chains of each isoform have a C-terminal coiled-coil region of approximately 600 amino acids, known as the long
arm, from which extend the separate N-terminal, so-called
short arms of each of the three constituent chains. The C-terminus of the chain extends beyond the C-termini of
the and chains and ends in a globular structure composed of five repeating units (3).
Laminin chains have diverse cellular interactions,
binding at least six integrins as well as other cell-surface
molecules such as dystroglycan (4, 5). The importance of
laminin chains is evident from diseases associated with
mutations of these chains, including a form of muscular
dystrophy with 2 mutations and junctional epidemolysis
bullosa, which is associated with mutations of 3 (6).
Laminins are expressed early in the developing lung
and are important for normal lung development, as deduced from studies with antilaminin antibodies and lung
buds in culture, and cocultures of epithelial and mesenchymal cells (7). With regard to laminin chains, laminins
2, 3, 4, and 5 are present in developing mouse lung
as shown by in situ hybridization at E15.5 and by Northern blot analysis of poly(A+)-selected RNA at E17.5 (2).
Laminin 1 has been reported in developing mouse, rabbit, and human lung tissue (12), and a short peptide sequence in the E8 region of the globular C-terminal domain
of laminin 1 promotes alveolar formation in cultures of
alveolar epithelial type II cells (16). However, laminin 1
was not found in a recent survey of laminin -chain expression in mouse lung, suggesting that other laminin chains may be predominant in lung (2).
In studies of -chain expression in lung, it has been
noted that the cellular localization of chain expression varies between chains. In situ hybridization of fetal mouse
lung revealed laminins 3 and 5 in epithelial buds and
laminin 4 in mesenchyme (2). To determine whether the
apparent differences in cellular expression of laminins 3,
4, and 5 observed in fetal lung persist in the adult lung,
we examined the expression of laminins 3, 4, and 5 by
isolated rat alveolar epithelial cells and rat-lung fibroblasts. We also investigated an immortalized rat alveolar
type II cell line. We observed that adult alveolar epithelial
cells express laminins 3 and 5, that adult lung fibroblasts
express laminin 4, and that an alveolar type II cell line expresses laminin 5.
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Materials and Methods |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Isolation and Culture of Lung Cells
Adult Sprague-Dawley rats were obtained from Charles River Laboratories (Cambridge, MA). After the animals were killed by pentobarbital injection, alveolar type II cells were isolated as previously described (17). Briefly, lungs were digested with elastase and the type II cells were purified by panning the cells over IgG-coated bacteriologic plastic dishes (Falcon; Becton Dickinson, Franklin Lakes, NJ). The cells were cultured in Dulbecco's modified Eagle's medium (DMEM) (GIBCO-BRL, Gaithersburg, MD) supplemented with 10% fetal bovine serum (FBS) (JRH Scientific, Lexana, KS) and 200 U/ml penicillin, 200 mg/ml streptomycin, and 0.5 µg/ml fungizone (Sigma Chemical Co., St. Louis, MO) at 1 × 107 cells per P-100 dish. Fetal, neonatal, and adult lung fibroblasts were isolated from minced lung tissue by collagenase digestion as described (18), and then cultured in DMEM/Ham's F12 medium (GIBCO) supplemented with 10% FBS, 200 U/ml penicillin, and 200 mg/ml streptomycin. All protocols used in the study were approved by institutional review boards.
Culture of a Rat Alveolar Type II Cell Line
Rat alveolar type II cells transfected with Simian virus 40 (SV40) large T antigen were kindly provided by Jerome S. Brody of the Boston University School of Medicine, Boston, MA (19). The cells were grown in minimal essential medium (MEM) (GIBCO) supplemented with 10% FBS, 200 U/ml penicillin, and 200 mg/ml streptomycin.
RNA Isolation and Northern Blot Analysis
Total RNA was isolated from cultured cells by guanidine
isothiocynanate extraction followed by phenol-chloroform extraction and ethanol precipitation, as previously
described (20). For Northern blot analysis of messenger
RNA (mRNA) expression, 10 µg of total RNA was denatured in 50% formamide, 1 M formaldehyde, 50 ng/ml
ethidium bromide at 68°C, then electrophoresed through a
1% agarose gel containing 1 M formaldehyde. RNA was
passively transferred to Hybond N+ membranes (Amersham, Arlington Heights, IL), fixed by treatment with 50 mM NaOH, hybridized, washed, and exposed as previously described (21). Complementary DNA (cDNA) probes
were radiolabeled by random priming with [32P]deoxycytosine triphosphate ([32P]dCTP). The cDNA probes used
to detect laminin 3, 4, and 5 mRNAs were as previously
described (22). Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) mRNA, used to normalize loading of
samples, was detected with a 1.3-kb rat cDNA insert. After washing, membranes were exposed to X-ray film at
70°C for 1 to 5 d with intensifying screens.
For Northern blot analysis of multiple tissues, filters containing poly(A+)-selected RNA from several adult mouse or rat tissues were hybridized according to the manufacturer's instructions (Clontech, Palo Alto, CA).
In Situ Hybridization
35S-labeled riboprobes were prepared from linearized cDNA templates for in situ hybridization of alveolar type II cells as described (22). A detailed description of the methods used for in situ hybridization of alveolar type II cells has been published previously (20).
Metabolic Labeling and Immunoprecipitation
Metabolic labeling and immunoprecipitation were done as
previously described (20). Briefly, alveolar type II cells,
obtained as described earlier, were cultured in DMEM
supplemented with 10% FBS in six-well culture plates
(Costar, Cambridge, MA) at 2 ml/well, 106 cells/ml. After
48 h, the cells were washed with methionine-free DMEM/
Ham's F12 medium, after which fresh medium containing
10% dialyzed FBS was added to each well, followed by 50 µCi of [35S]methionine (ICN Biomedical, Costa Mesa,
CA). The cultures were returned to a 5% CO2 incubator
for 24 h, after which the conditioned media were collected.
Supernatants were stored at 80°C. Newly synthesized
laminin 5 was determined over other 24-h intervals, including Days 2 to 10. Similar procedures were used to label lung fibroblasts, except that the cells were labeled at a
single time point.
Antibodies raised to recombinant laminin 4 or 5
polypeptides expressed in bacteria (2) were used to immunoprecipitate conditioned media or cell extracts. Each of
these antibodies reacts specifically with a single laminin chain and does not cross-react with other laminin chains.
Conditioned media were mixed with specific antibody or
preimmune serum, incubated for 1 h at 37°C, and then incubated overnight at 4°C. The immune complexes were
separated by the addition of protein A sepharose (Zymed
Laboratories, San Francisco, CA) and incubation for 30 min at room temperature. The pellets were washed, resuspended in electrophoresis buffer, incubated at 60°C for 15 min, and microcentrifuged, and the supernatants were
transferred to new tubes. -Mercaptoethanol was added to a final concentration of 2%; the samples were boiled for 5 min and subjected to polyacrylamide gel electrophoresis
(PAGE) in 7.5% gels. Gels were incubated for 30 min at
room temperature in Amplify (Amersham), rinsed with
water, dried, and exposed to autoradiographic film.
Immunohistochemistry
Immunofluorescence staining of fresh-frozen adult rat lung tissue was done on 7-µm-thick cryostat sections, using the same antibodies and methods as previously described (2). The lung was inflated by injection of OCT compound (Sakura Finetek USA, Inc., Torrance, CA) into the trachea prior to sectioning. Antibodies were diluted in 1% (wt/vol) bovine serum albumin (BSA) in phosphate-buffered saline (PBS) and incubated on sections for 1 to 2 h. After rinsing away the unbound primary antibody with PBS, secondary antibodies were applied for 1 to 2 h. Sections were rinsed again, and then mounted in glycerol-phenylediamine and observed with epifluorescent illumination.
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Results |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Expression of Laminin 3, 4, and 5 mRNAs in Lung
To demonstrate the expression of laminin 3, 4, and 5
mRNAs in adult mouse and rat lung relative to other organs, we hybridized multiple tissue poly(A+) RNA blots
with 32P-labeled cDNA probes specific for these laminin chains (Figure 1). Some differences in expression patterns
of laminin chains were observed in mouse and rat tissues. Among mouse tissues, laminin 3 mRNA was detected primarily in lung. Two molecular-weight species of
laminin 3 transcripts were observed, at approximately 5.5 kb and 10 kb, respectively. In contrast, laminin 3 mRNA
was present at low levels in rat lung, and was most prominent in spleen. In rat tissues, laminin 3 was detected as a
single band of approximately 6 kb except in spleen, where
heterogeneity in molecular weight was apparent. In the
mouse, laminin 4 mRNA was expressed at highest levels
in the lung, and was also detected in the heart and skeletal muscle. In the rat, laminin 4 mRNA was highly expressed
in both lung and heart. In the mouse, laminin 5 mRNA
was predominant in the lung, but was also present in kidney, skeletal muscle, and heart. Two transcripts, of approximately 11 kb and 13 kb, were detected in all of these
tissues. Expression of these laminin chains was not detected
in brain, spleen, liver, or testis. In the rat, a single laminin 5
mRNA transcript of approximately 12 kb was prominent
in the lung, but was also present in kidney and heart. Autoradiography for 3 to 5 d was required for detection of
signal for these laminin -chain mRNAs. Hybridization
with a probe for -actin mRNA (autoradiographic exposure: 1.5 h) showed some differences in loading between
samples, but revealed the presence of mRNA in each lane.
As anticipated, hybridization to mRNAs of other actin isoforms was evident in heart and skeletal muscle.
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Expression of Laminin 3 and 5 mRNAs by
Alveolar Epithelial Cells
We next examined the expression of laminins 3, 4, and
5 in adult rat alveolar type II cells at 1 to 6 d in culture.
Laminin 3 mRNA was expressed at all time points, with
some decline in level of expression at the later time points
(Figure 2). Similarly, laminin 5 mRNA was detected
throughout the time course of the experiment. In contrast,
expression of laminin 4 mRNA was not detectable by
Northern blot analysis of total RNA from alveolar type II
cells at any time point.
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Production of Laminin 5 by Alveolar Type II Cells
To assess synthesis and secretion of laminin 5 by cultured
alveolar type II cells, cultures were metabolically labeled
with [35S]methionine for 24 h, after which media were harvested for immunoprecipitation (Figure 3). Immunoprecipitation with immune serum yielded a unique band at
approximately 400 kD (Figure 3, arrowhead), which was not seen with preimmune serum, and which was consistent
with the predicted size of laminin 5. Laminin 5 expression was evident throughout the time course of the experiment.
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Uniform Expression of Laminin 5 mRNA by
Alveolar Type II Cells
To determine whether the laminin 5 production we detected in cultured alveolar type II cells was due to a contaminating subpopulation of cells, we analyzed its expression at the cellular level. Cells were cultured on glass slides
for 4 d and then fixed for in situ hybridization. As shown
(Figures 4A and 4B), signal for laminin 5 mRNA was detected in nearly all cells in these cultures.
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Laminin 4 mRNA Expression by Lung Fibroblasts
We next examined the expression of mRNAs for laminins
3, 4, and 5 in fibroblasts isolated from the lung parenchyma of 4-d and 10-d-old neonatal and adult rats. Expression of laminin 4 mRNA was seen in neonatal and adult
lung fibroblasts (Figure 5). Faint signal for laminin 5
mRNA expression was observed in neonatal lung fibroblasts, but was less evident in total RNA isolated from adult lung fibroblasts. In no assay was there detectable
laminin 3 mRNA in lung fibroblasts.
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Production of Laminin 4 by Lung Fibroblasts
Metabolic labeling and immunoprecipitation of medium
conditioned with rat lung fibroblasts with antibody to mouse
laminin 4 chain revealed the presence of three bands not
observed in the preimmune serum-precipitated sample (Figure 6). Immunoprecipitation for laminin 5 did not show
expression of this chain in cultured lung fibroblasts.
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Expression of Laminin -Chain mRNAs by
Immortalized Alveolar Type II Cells
Northern blot analysis of RNA from SV40T-immortalized
rat alveolar type II cells showed expression of laminin 5
(Figure 7), but signal for laminin 3 or 4 was not detected
(data not shown).
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Immunolocalization of Laminin Chains in
Adult Rat Lung
Having determined that laminin 4 and 5 mRNAs were
present in lung tissue and were expressed in culture by
lung fibroblasts and alveolar type II cells, respectively, we
next examined the localization of laminin 4 and 5 chains
relative to laminin 1 and 2 chains in adult rat lung tissue
by immunofluorescence staining (Figure 8). Staining for
laminin 4 and 5 chains was abundant in nearly all basement-membrane zones of the lung (Figures 8A and 8B). In
serial sections, laminin 1 and 2 chains (Figures 8C and
8D) were detected in patterns that were not completely overlapping with each other, but in the same zones as
laminin 4 and 5 chains. In addition, in accord with published data (14), laminin 1 was detected throughout the
lung (data not shown). Thus, laminin 4 and 5 chains may
associate with laminins 1, 2, and 1 in lung basement
membranes to produce laminin isoforms 8 to 11.
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Discussion |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminin was originally identified in 1979 as a heterotrimer
of polypeptide chains called A, B1, and B2 (23, 24), which are designated 1, 1 and 1, respectively, in current laminin nomenclature (25). The first homologue of the 1
chain, 2, was isolated in 1990 (26). Subsequently, three
other homologues have been found. All of the five known
laminin chains assemble into laminin heterotrimers (2).
In the mouse, the genes encoding the chains are located
on four different chromosomes.
With respect to lung, a number of observations have
been made about laminin chains. Laminin 1 is not expressed in adult mouse lung, and in our previous studies
was not evident in fetal mouse lung at 15.5 d by in situ hybridization or at 17 d by ribonuclease protection (2). However, these findings are at variance with those in other
studies showing laminin 1 in developing lung (12), and
in cocultures of epithelial and mesenchymal cells derived from developing mouse lung. With these latter observations it was reported that laminin 1 production requires
direct contact between epithelial and mesenchymal cells,
and is detectable adjacent to lung buds, where there is epithelial-mesenchymal cell contact (15). Furthermore, treatment of fetal mouse lung mince cultures with antibodies
specific for laminin 1 caused loss of smooth-muscle -actin
and changes in cell morphology in bronchial smooth muscle (15). These observations support a role for laminin 1
in the morphologic development of fetal lung. Nonetheless, it seems clear that the laminin 1 chain, which is the
laminin chain produced by the Engelbreth-Holm-Swarm
(EHS) tumor cell, is not present in adult mouse lung. This
finding suggests that EHS basement membrane should not
be considered an authentic replica of mouse alveolar basement membrane at all stages of lung development. In this
context, it should be noted that the monclonal antibody
4C7, which has been used to investigate the distribution of
laminin 1 (13, 14), recognizes laminin 5 rather than laminin 1 (2, 27).
Laminin 2 presents a different situation. Laminin 2 is
evident in E15.5 mouse embryo lung by in situ hybridization, and is expressed in 17.5-d fetal lung and adult lung, as
determined by ribonuclease protection (2). It has also
been observed inconsistently by immunohistochemistry in
epithelial structures in preglandular human fetal lung buds
and in bronchial smooth muscle at the canalicular stage
(14). In adult mouse lung, however, laminin 2 was not detectable through immunohistochemical analysis (2). Similarly, laminin 2 is not apparent in adult human lung (14).
Expression of laminin 2 therefore appears to be confined
to development in normal lung. The basis for the loss of
immunoreactive laminin 2 in adult mouse and human
lung despite its expression during lung development remains unclear, but illustrates the complexity in the expression of laminin isoforms in tissues at different stages of
maturation. Interestingly, laminin 2 expression was detected in basement membrane in bronchial biopsies from
individuals with severe asthma, suggesting that its expression can be reinitiated in states in which there may be
basement-membrane injury and accelerated turnover (28).
The mouse laminin 3 gene encodes at least two polypeptides, laminin 3A and laminin 3B. Both polypeptides
share the same C-terminus, but laminin 3A is truncated as
compared with laminin 3B, lacking a number of domains
at the N-terminus. In adult mouse lung tissue, the laminin
3B mRNA isoform was predominant in comparison with
that for laminin 3A, resembling the results obtained by Galliano and associates (29). However, a band corresponding to the 3A isoform was clearly present in lung. In
rat tissues, laminin 3 mRNA was detected as a single
band of approximately 5.5 kb, which probably corresponds
to laminin 3A. In contrast to the pattern of expression
seen in mouse tissues, laminin 3 mRNA was predominant
in spleen, where heterogeneity in its molecular weight was
noted. Little laminin 3 expression was detected in adult
rat lung, indicating species-specific patterns of laminin -chain expression in the rat and mouse. In our analysis of
laminin 3 expression by cultured rat alveolar type II cells,
expression of the laminin 3A isoform was predominant,
but some laminin 3B isoform was detected. Laminin 3 associated with 1 and 1 chains would form laminin-6, and
in association with 1 and 2 would form laminin-7.
Like laminin 3A, but in contrast to other laminin chains, laminin 4 is truncated at the N-terminus. In our
study, as well as in previously published data (2, 30), expression of laminin 4 was particularly prominent in both
fetal and adult mouse lung, with expression also seen in
other tissues, including heart and muscle. Lung is a prominent site of expression of laminin 4 in studies of human
fetal and adult tissues (31, 32). In situ hybridization shows
laminin 4 expression as limited to mesenchyme in developing mouse lung and kidney (2), and in human neonatal lung laminin 4 is found in alveolar mesenchymal cells,
whereas alveolar epithelial and endothelial cells are negative for this laminin chain (31). These findings are entirely
consistent with our observation that lung fibroblasts express laminin 4 and secrete laminin 4 protein, whereas
alveolar type II cells do not. This finding also represents
an example of an alveolar basement membrane component that is produced principally or exclusively by alveolar mesenchymal cells. Entactin is another example (20, 33).
We observed three polypeptides immunoprecipitated by
antiserum to laminin 4. These may represent the products
of posttranscriptional modifications such as processing,
similar to that observed for laminin 3 (34). Immunostaining of laminin 4 in adult rat lung was evident throughout
alveolar walls, and overlapped with immunostaining for
both laminin 1 and 2. In lung extracts, laminin 4 has
been found in association with 1 and 1 chains, forming
laminin-8, and in association with laminin 1 and 2 chains,
forming laminin-9 (2).
Laminin 5 is the largest laminin chain (35). Its large
size is due to several larger domains in the short arm. The
short arm of laminin 5 is also notable for its resemblance
to the short arm of the only Drosophila laminin chain,
leading to speculation that laminin 5 is the ancestral mammalian laminin chain. Laminin 5 is expressed widely in
both fetal and adult tissues and, as with laminin 4, is prominently expressed in lung. The expression is highly linked to
development, occurring late in epithelial- and endothelial-cell maturation and early in embryogenesis in muscle-fiber
basement membranes of skeletal muscle (36). Interestingly, we detected transcripts of laminin 5 of two distinctly different sizes in adult mouse tissues, one at 11 kb
and another, less prevalent, at approximately 13 kb. In
adult rat tissues we detected a single band of approximately 12 kb. In cultured rat alveolar type II cells we detected a single band at approximately 11 kb. The small differences in size of laminin 5 mRNA in adult rat tissues
and cultured alveolar type II cells is probably due to difficulty in the size estimation of high-molecular-weight
mRNAs. During development there appear to be changes
in the expression of laminin 5 relative to that of other
laminin chains, especially 1. For example, in assembly
of the glomerular basement membrane there is initially
prominence of laminin 1, which later diminishes as laminin 5 appears (2, 37). A detailed analysis of laminin 5 expression in the developing mouse lung is in progress in our laboratory.
The present study shows that adult rat alveolar epithelial cells in culture express laminin 5 mRNA and produce
laminin 5 protein. These findings are consistent with the
results of previous in situ hybridizations of E14 and 15.5-d
mouse embryos (2, 37). Alveolar type II cells showed increased expression of laminin 5 with increasing days in
culture. The low laminin 5 signal found by in situ hybridization in freshly harvested cells fits with the low level of
signal in adult mouse lung, and suggests minimal constitutive expression of laminin 5 in the normal adult lung. The
basis for increased expression of laminin 5 with time in
culture remains to be determined. Only a low level of
laminin 5 signal was detected with a rat alveolar type II
cell line, a finding that is difficult to interpret. The weak
signal could be equivalent to the freshly harvested alveolar
type II cell or may represent a deficiency in the phenotype
of these cells in comparison with normal alveolar type II
cells. As with laminin 4, immunostaining of adult rat lung
for laminin 5 showed it to be evident throughout alveolar
walls, and overlapping immunostaining of both laminin 1
and 2. Laminin 5 associated with 1 and 1 chains would
form laminin-10, and in association with 1 and 2 would
form laminin-11.
These studies indicate that although the cellular origins
of laminin 4 and 5 chains are different, these chains are
present throughout alveolar basement membranes. On the
basis of the colocalization of laminin 4 and 5 chains with
1 and 2 chains, it is likely that alveolar basement membranes of the adult rat lung, like those of mouse lung (2),
contain laminins 8 to 11. How particular cell-type-specific
laminin isoforms are incorporated throughout alveolar
basement membranes is currently unclear.
Recovery from diffuse alveolar damage, a situation in
which there is alveolar basement membrane destruction
(38), suggests that the adult human lung can reinitiate
or markedly upregulate synthesis of alveolar basement
membrane components. Because laminin 2 expression appears to be normally confined to lung development, its
presence in adult lung may be an indicator of active basement-membrane production. Because laminin 4 is exclusively a mesenchymal product and laminins 3 and 5 are
epithelial in origin, it should be possible to elucidate the
relative contributions of these cell types to alveolar repair
by analysis of expression of these laminins. In this regard, the idea that fibroblasts, by laying down interstitial
collagens, are detrimental to alveolar repair may not take
into account the importance of some fibroblast products, such as laminin 4, in reconstitution of the alveolar basement membrane.
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Footnotes |
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Address correspondence to: Robert M. Senior, M.D., Pulmonary and Critical Care Medicine, Barnes-Jewish Hospital (North Campus), 216 South Kingshighway, St. Louis, MO 63110. E-mail: rsenior{at}imgate.wustl.edu
(Received in original form July 14, 1997 and in revised form January 13, 1998).
Acknowledgments: This work was supported by grants from the National Institutes of Health, including Program Project HL 29594, and the Alan A. and Edith L. Wolff Charitable Trust. The authors thank Dr. Sarah Dunsmore, Ph.D., for review of the manuscript.
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References |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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