 1 and 5 in Human Lung
during Development
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Abstract |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminins are trimeric glycoprotein components of basement
membranes. Each laminin has three structurally similar chains,
designated 
, 
, and 
. Five laminin chains are now known.
In previous studies using monoclonal antibody 4C7, laminin
1 was thought to be present in basement membranes of human lung throughout development and in the adult, but recent expression studies have demonstrated that 4C7 identifies
laminin 5 rather than 1. To determine the temporal and
spatial patterns of laminin 1 and laminin 5 in developing
human lung, we prepared complementary DNA probes specific for laminin 1 and 5 messenger RNAs (mRNAs). By
Northern analysis, laminin 1 mRNA was prominent in first-trimester fetal lung, but was not detectable at 23 wk or at
later times. In contrast, laminin 5 mRNA was readily detected in early fetal lung and remained present thereafter. Immunohistochemical staining demonstrated laminin 1 only in
early fetal lung, whereas laminin 5 was persistent from the
early fetal period. In situ hybridization localized laminin 1 expression to distal epithelium in the first-trimester lung, and
laminin 5 to all epithelium and developing pulmonary arteries from the first trimester through the perinatal period.
These studies indicate that laminin 1 expression is restricted
to early human lung morphogenesis, whereas the expression
of laminin 5 in human lung is continuous from early lung development through adult life. It is evident that laminin 1 and
laminin 5 have different roles in the development of the human lung.
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Introduction |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminins are high molecular-weight, cruciform heterotrimeric glycoproteins found in all basement membranes,
where they form a network connected by entactin (or nidogen) to the type IV collagen network (1). The discovery
and characterization of laminin was facilitated by its abundance in the Engelbreth-Holm-Swarm extracellular matrix (2, 3). For some time, the diversity of vertebrate laminins was unknown, and it was assumed that laminin was
always comprised of the prototypical A (1), B1 (1) and
B2 (1) chains, which form a trimer now known as laminin-1. Multiple laminin [4], [3], and [3] chains have
now been identified in mammals, and these form up to 12 different laminin isoforms, which are differentially expressed in various tissues (5). Among laminin chains,
laminin 5 is the largest and is most closely related to the
most abundantly expressed Drosophila laminin chain (4).
Laminin 5 is widely expressed in vertebrate tissues (4).
Perturbing basement membrane assembly in lung bud
cultures with anti-laminin 1 antibodies results in arrest of
branching morphogenesis, suggesting a primary role for
this chain in lung development (6). Expression of laminin
1 messenger RNA (mRNA) has been reported in fetal
lung tissue, but not in adult mouse lung tissue (7). However, numerous studies using 4C7, a monoclonal antibody
(mAb) directed against a laminin chain, have reported staining of basement membranes of adult human lung. 4C7
was originally thought to recognize laminin 1, but is now
known to recognize human laminin 5 (8). Accordingly,
the timing and localization of laminin 1 expression in human lung has not been determined. In this study, we determined the expression pattern of laminin 1 in human lung
tissue and contrasted it with 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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Lung Tissue
Human fetal lungs, 54 to 101 d of gestation, were obtained from the Central Laboratory for Human Embryology (University of Washington, Seattle, WA). For Northern blotting and reverse transcriptase/polymerase chain reaction (PCR), the lungs were frozen in liquid nitrogen immediately upon collection and shipped on dry ice. For immunohistochemistry, the lungs were immersed in Tissue-Tek O.C.T. Compound (Sakura Finetek, Torrance, CA), frozen in liquid nitrogen upon collection, and shipped on dry ice. For in situ hybridization, the lungs were put into phosphate-buffered formalin (10%vol/vol) immediately upon collection and shipped on wet ice. Neonatal lung tissue and adult lung tissue were obtained from the Department of Pathology at Barnes-Jewish Hospital at Washington University Medical Center. Institutional review boards approved all protocols.
Molecular Probes
The complementary DNA (cDNA) probe for human laminin 1
was generated by PCR from the full-length human laminin 1
cDNA (provided by Peter Yurchenco, UMDNJ/Robert Wood
Johnson Medical School, Piscataway, NJ). The probe consisted of
nucleotides 2027-2556 (GenBank Accession number X58531)
cloned into pBluescript II KS (Stratagene, La Jolla, CA). The
cDNA probe for human laminin 5 was an Image Consortium
expressed sequence tag cDNA clone (EST) 342926, GenBank
Accession number W67855. This EST encodes a portion of the
COOH-terminal G domain.
Northern Blot Analysis
To assess laminin chain mRNA expression in first-trimester
lung, total RNA was isolated from frozen specimens, electrophoresed through formaldehyde-containing agarose gels, transferred
to charged nylon membranes, hybridized with radiolabeled cDNA
probes, and exposed by autoradiography as we described previously (9). For Northern analysis of multiple tissues, filters containing poly (A+)-selected RNA from pools of tissue RNAs from nine
fetal (~ 161 d of gestation) or five adult subjects were hybridized
according to the supplier's instructions (Clontech, Palo Alto, CA).
Immunohistochemistry
Immunofluorescent staining of fetal and adult lung tissue was done
using antibodies and methods identical to those described previously (10). mAb to laminin 5, 4C7, was isolated from ascites induced with hybridomas provided by Eva Engvall (The Burnham
Institute, La Jolla Cancer Institute, La Jolla, CA), (11). Donald
Gullberg (Uppsala University, Uppsala, Sweden) and Peter Ekblom (Lund University, Lund, Sweden) provided anti-hLN-1G4/
G5, a polyclonal antibody to laminin 1 (8). Lung specimens were
embedded in Tissue-Tek O.T.C. Compound, then sectioned at 4 to
8 µm on a cryostat. Antibodies were diluted in 1% (wt/vol) bovine
serum albumin in phosphate-buffered saline (PBS) and incubated
on sections for 1 to 2 h. After rinsing the unbound primary antibody with PBS, secondary antibodies were applied for 1 to 2 h.
Sections were rinsed again, then mounted in gycerol-para-phenylediamine and observed with epifluorescent illumination. A mAb to
thyroid transcription factor (TTF)-1 was purchased from DAKO
Corporation (Code No. M3575, Carpinteria, CA) and used as directed by the manufacturer.
In Situ Hybridization
[35S]-labeled riboprobes were prepared from linearized laminin 5
and 1 cDNA templates for in situ hybridization of fetal and adult
human lung specimens as described (9). A detailed description of
the methods used for in situ hybridization has been published previously (12). Sense controls were included with each hybridization and
were handled identically to the corresponding antisense samples.
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Results |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Laminin 1 Expression Is Restricted to Early Fetal Lung
To determine the expression patterns of laminin 1 and 5
in developing human lung, we isolated total RNA from
human fetal lungs, 72 to 101 d of gestation, and hybridized
Northern blots for laminin 1 and 5 mRNAs (Figure
1A). A band corresponding to laminin 1 mRNA, migrating at approximately 10 kb, was readily detected in all
samples by Northern analysis, with an apparent peak in
expression at around 94 d of gestation. Signal for laminin 5 mRNA, appearing as a single band at approximately 11 kb, was prominent between 72 and 94 d gestation and declined thereafter. In an alveolar type II cell-like carcinoma
cell line, A549 cells (American Tissue Type Culture Collection, Rockville, MD), prominent signal for laminin 5
was noted but no laminin 1 mRNA was detected, as reported by Kikkawa and colleagues (13).
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Next, we hybridized radiolabeled cDNA probes specific for these laminin chain mRNAs or -actin to Northern blots containing poly A+ mRNA from a pool of fetal
tissues of approximately 23 wk gestation (Figure 1B). At
this stage, laminin 1 mRNA was not detected in lung but
was abundant in kidney. In contrast, laminin 5 mRNA
was prominent at 23 wk of gestation in kidney and lung, and was also detected in brain. In a multitissue blot of
mRNA isolated from adult human tissues, laminin 1
mRNA was not detected by Northern analysis, showing
that this laminin chain has a limited expression pattern
in adult human tissues (Figure 1C) similar to that in the
adult mouse (7). In contrast, laminin 5 mRNA was abundant in placenta; at moderate levels in lung, kidney, and pancreas; and at low levels in heart, liver, and skeletal muscle.
Immunohistochemical Localization of Laminin
1 and 5 in Human Lung
Antisera specific for human laminin 1 and 5 were used
to localize their presence in fetal and adult human peripheral lung specimens. Anti-hLn-1G4/G5A, a polyclonal
antibody raised against recombinant laminin 1 (8),
stained human fetal lung basement membranes at 85 d of
gestation, outlining airways (Figure 2A), but did not stain
alveolar basement membranes in adult human lung (Figure
2B). In contrast, 4C7, a mouse mAb specific for laminin 5
(8), stained both fetal and adult lung basement membranes (Figures 2C and 2D). Deposition of laminin 5 into the
basement membranes of fetal and adult human lung followed the pattern we anticipated on the basis of the presence of this mRNA in lung at both stages of development.
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In Situ Hybridization for Laminin 1 mRNA in
Fetal Human Lung
To expand our study of laminin 1 and 5 expression in
fetal lung, samples of formalin-fixed fetal lung tissue from
different gestational ages and from postnatal lung were
hybridized in situ for laminin 1 and 5 mRNAs. At 85 d
of gestation, which corresponds to the pseudoglandular
stage of human lung development, signal for laminin 1
mRNA was detected in distal, columnar epithelium of
branching airways (Figure 3B). In contrast, cuboidal epithelial cells in central regions of distal cruciform airway
did not express laminin 1. Loose mesenchyme surrounding airways was essentially devoid of signal, as were tracheal cartilage, vascular smooth muscle, and pleura (not
shown). Signal for laminin 1 was not detected in at any
site in distal lung at 101 d of gestation (Figure 3D) or in
neonatal lung (Figure 3F). These data indicate that laminin 1 expression is confined to a narrow period of human lung development preceding the canalicular stage and that
it is confined to the most distal portion of the developing
airway system during that period.
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Disparate Expression Patterns of Laminin 1 and
TTF-1 in Early Fetal Human Lung
Noting that laminin 1 expression in early fetal lung was
confined to distal epithelium, we compared the expression
patterns of laminin 1 and TTF-1. TTF-1 marks distal lung
epithelium (14, 15) and activates transcription of several
lung-specific genes, including surfactant protein A and B
genes (16). At 85 d of gestation, laminin 1 expression
was confined to the most distal regions of epithelial buds,
in cells with a columnar morphology (Figures 4A and 4B).
Immunohistochemical staining for TTF-1 was less restricted,
marking both central, cuboidal epithelium of branching
airways and distal, columnar epithelium of columnar airways (Figure 4C). However, columnar epithelium of proximal bronchi stained only marginally for TTF-1.
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In Situ Hybridization for Laminin 5 mRNA in Fetal
and Neonatal Human Lung
In contrast to the limited temporal pattern of expression
of laminin 1, laminin 5 expression was found in late
first-trimester, second-trimester, and neonatal lung specimens (Figure 5). At 85 d of gestation, signal for laminin 5
was present in all epithelium. Nonvascular mesenchyme
between airways also showed some signal for laminin 5
(Figure 5B). At 19 wk of gestation, prominent signal for
laminin 5 was found in the smooth-muscle layer of large
pulmonary arteries as well as in virtually all epithelium
(Figures 5C and 5D). In neonatal lung at 9 d, signal for
laminin 5 was found in alveolar walls, where it localized
to cells with a location and morphology consistent with
type II epithelial cells (Figures 5E and 5F). At this stage,
signal within pulmonary arteries was much reduced, and
bronchial epithelium was negative (not shown). In adult
lungs a few positive cells were detected per high-power field, but no consistent pattern implicating a particular
compartment or cell type was found (data not shown).
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Discussion |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Previous studies of laminin chain expression in the developing human lung antedated the discovery of laminin 5 and
the recognition that mAb 4C7 identifies laminin 5 rather
than laminin 1. Lallemand and colleagues studied 20 normal
fetal lungs ranging in age from 8 to 38 wk by in situ hybridization and by immunohistochemical staining (19). They observed that mRNAs for 1 and 1 chains were already
present at the earliest fetal ages, principally in epithelium,
with 1 chain expression more prominent. This pattern persisted during the late psuedoglandular stage when prominent signals were seen in mesenchymal cells adjacent to epithelium as well in the epithelial cells. After the twenty-fourth
week, signals were strong in alveolar walls for 1 and 1
chains by in situ hybridization but it was not possible to distinguish the cell types expressing these chains by light microscopy because of the thinness of the alveolar walls. Immunohistochemistry revealed uniform staining of epithelial tips
early, but later in gestation there were disruptions of staining
at the tips, suggesting possible degradation at those sites.
Virtanen and colleagues used immunohistochemistry to
study the expression of laminin , , and chains in human
fetal lung at 14 to 16 and 19 to 21 wk of gestation, corresponding respectively to the late pseudoglandular and canalicular stages of lung development (20). Prominent staining
with antibody presumptively recognizing laminin 1 was
seen in the pseudoglandular epithelial bronchial buds and
larger bronchi. The authors noted the discrepancy between the distinctive immunostaining for laminin 1 in their studies and the minimal expression of laminin 1 chain mRNA by
in situ hybridization and Northern blotting. A logical explanation at the time was that slow turnover of laminin would
account for the presence of laminin 1 protein with little
laminin 1 mRNA. In retrospect, the explanation for the
discrepancy is that the mAb used, 4C7, does not recognize
the laminin 1 chain but instead is specific for the laminin 5
chain. By substituting 5 for 1, the results of this report offer valuable information about expression patterns of laminin 5 in human lung. Laminin 5 was found in virtually all
lung structures at both developmental time points and in
adult alveoli and bronchi. Thus, the results agree with the
present study that laminin 5 is present in the developing human lung in the early pseudoglandular stage.
In the present study, laminin 1 was found in lung basement membranes only during the early pseudoglandular
stage of development, and was undetectable in midgestation, neonatal, and adult lung specimens. These findings
match recent observations in the normal adult mouse in
which laminin 1 expression histochemically was restricted
to epithelial basement membranes in the urinary tract, reproductive organs, pia mater, adrenal gland, matrices covering the vitreous chamber and lens of the eye, and Brunner's glands in the gut (7). Notably, immunostaining of
lung was negative, including the large airways and trachea.
In first-trimester fetal lung we localized laminin 1 by
immunohistochemistry to the basement membranes of virtually all airways, but by in situ hybridization the expression was confined to distal epithelium of lung buds. Thus,
laminin 1 must have been expressed at these other locations at a previous stage and time. These findings support
a model in which laminin 1 is likely the primary chain found in the early basement membrane that forms around
growing epithelial buds as they invade the surrounding
mesenchyme. The laminin 1-rich basement membrane
may be important for anchoring epithelial cells and establishing their polarity, as well as determining the architecture of the airways. As epithelial cells become proximal and differentiate, they change their laminin chain expression patterns. Sorokin and coauthors also found this
expression pattern in mouse lung (21). The switch from expression of laminin 1 and laminin 5 to laminin 5 alone
would result in epithelial basement membranes transitioning from containing laminins -1, -10, and -11 to containing
laminins -10 and -11. These changes could be important in
regulating epithelial cell proliferation, shape, and phenotype by cell-matrix signaling events.
Recent studies indicate that different cell types may use
a variety of cell-surface receptors to attach to laminins containing an 5 chain, namely laminins -10 and -11. Eble and
coworkers ectopically expressed soluble 3 and 1 integrin
heterodimers in insect cells and found that these strongly
bound laminin-5 and laminin-10, but not laminin-1 or laminin-2 (22). A549 cells,which express laminin 5, strongly
adhere to laminin 10/11. Antibodies to integrin subunits 3
and 1, but not to subunits 2 or 6, blocked this adhesion
(13). In two other epithelial cell lines, antibodies to dystroglycan and the integrin subunit 6, but not to subunits 3
or 1, blocked adhesion (23). Tani and coauthors reported that different choriocarcinoma cell lines use either integrin subunits 6 or 3 to attach to laminin 10/11 (24). It has recently been shown that in bone marrow, laminin 2, 4,
and 5 are expressed, but not laminin 1, and the integrin
receptor 61 mediates cell adhesion to 5-containing
laminins by a mouse hematopoietic mixed cell line (25).
Thus, it appears that 3, 1, 6-containing integrins, and
dystroglycan may be used by different cells to adhere to
5-containing laminins -10 and -11. In contrast, numerous cell surface receptors have been reported for laminin-1, including dystroglycan and integrins 61, 64, 11, 21,
and 71. Changing from a laminin-1-rich basement membrane to a laminin-10/11-rich basement membrane could
alter cellular phenotype through cell-matrix interactions involving changes in receptor signaling during development. In this context, Schuger and colleagues discovered that the
expression of laminin 1 by fetal mouse lung cells in culture, harvested from embryos at Day 15 of gestation, required contact between epithelial and mesenchymal cells
and then both cell types produced laminin 1 (26). A role
for laminin 1 was suggested in their studies involving lung
explants harvested at Day 12 of gestation. Inclusion of
mAbs to laminin 1 in these cultures blunted polarization of peribronchial cells. The authors suggested that laminin
1 may play a role in the development of the smooth-muscle phenotype in bronchial smooth muscle.
Although laminin 5 colocalizes with laminin 1 in epithelium in the early fetal lung, it is clear that laminin 5 is
also expressed in cell types that do not, at an earlier stage,
express laminin 1. For example, vascular smooth-muscle
cells in developing human lung express laminin 5, but
laminin 1 was not detected in these cells at any stage of
lung development. This pattern of arterial expression is
also found in the developing kidney (10). In contrast to
vascular smooth muscle, airway smooth muscle was not
found to express either the laminin 1 chain or the laminin 5 chain at any stage of human lung development.
In summary, laminin 1 has a highly restricted spatial
and temporal expression pattern during lung development. The differences between its expression and that of
laminin 5 indicate that these chains of laminin trimers
have important different structural and/or signaling roles.
The developing lung provides an excellent model to explore the basis for the differences in expression patterns of
basement membrane components.
Addendum: While the present report was in review, a related paper was published (27); this study shows immunohistochemically that laminin 1 is present in distal bronchial tubular epithelial basement membrane at 16 to 19 wk
of gestation, but not later.
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Footnotes |
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Address correspondence to: Robert M. Senior, M.D., Barnes-Jewish Hospital, 216 S. Kingshighway Blvd., St. Louis, MO 63110. E-mail: seniorr{at}msnotes.wustl.edu
(Received in original form April 7, 2000 and in revised form September 8, 2000).
Abbreviations: complementary DNA, cDNA; monoclonal antibody, mAb; messenger RNA, mRNA; thyroid transcription factor, TTF.Acknowledgments: This work was supported by grant HL29594 from the National Heart, Lung and Blood Institute of the National Institutes of Health, and by the Alan A. and Edith L. Wolff Charitable Trust.
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References |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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