ARTICLE |
Correspondence to: Peter Ekblom, Dept. of Animal Physiology, Uppsala Univ., Biomedical Center, Box 596, S-751 24 Uppsala, Sweden.
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Summary |
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Dystroglycan is a cell surface protein which, in muscle, links the extracellular matrix protein laminin-2 to the intracellular cytoskeleton. Dystroglycan also binds laminin-1 and the binding occurs via the E3 fragment of laminin-1. Recently, it was found that dystroglycan is expressed in developing epithelial cells of the kidney. Moreover, antibodies against dystroglycan can perturb epithelial development in kidney organ culture. Therefore, dystroglycan may be an important receptor for cellmatrix interactions in non-muscle tissues. However, information about the tissue distribution of dystroglycan is limited, especially in adult tissues. Here we show that dystroglycan is present in epithelial cells in several non-muscle organs of adult mice. Dystroglycan is enriched towards the basal side of the epithelial cells that are in close contact with basement membranes. We suggest that dystroglycan is involved in linking basement membranes to epithelial and muscle cells. Dystroglycan may be important for the maintenance of tissue integrity. (J Histochem Cytochem 46:449457, 1998)
Key Words: dystroglycan, laminin-1, laminin-2, epithelial cells
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Introduction |
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INTERACTIONS between cells and the extracellular matrix are important for organ development and for maintenance of tissue architecture. Dystroglycan is a recently characterized high-affinity binding protein for many laminins, the major glycoproteins of basement membranes. Dystroglycan was originally identified as a part of a complex of proteins, termed the dystrophinglycoprotein complex (DGC), which in muscle anchors dystrophin to the sarcolemma. Dystroglycan is encoded by a single messenger RNA that by post-translational processing forms the extracellular 156-kD -subunit (
-dystroglycan) and the 43-kD transmembrane ß-subunit (ß-dystroglycan). In muscle, laminin-2 binds
-dystroglycan, which in turn is non-covalently attached to ß-dystroglycan which, through its cytoplasmic tail, binds directly to the C-terminal portion of dystrophin. Therefore, dystroglycan is believed to form an important structural link between the cytoskeleton and the extracellular matrix in muscle (
Several proteins of the DGC are muscle-specific, but Northern blot analyses have shown that dystroglycan is expressed in a wide variety of non-muscle tissues (
It is therefore obvious that dystroglycan may be an important receptor for cellmatrix interactions in non-muscle tissues. A targeted disruption of the dystroglycan gene in mice resulted in early embryonic lethality. In dystroglycan null mice, Reichert's membrane is disrupted, suggesting a role for dystroglycan in basement membrane assembly (
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Materials and Methods |
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Immunofluorescence
Mouse tissues from adult male C57 bl/6J hybrid mice and mammary glands from pregnant NMRI hybrid mice were frozen in Tissue Tek. The pregnant uteri were isolated from C57bl/129Sv hybrid mice, fixed in 4% paraformaldehyde, and embedded in paraffin. Human kidney biopsy specimens were kindly provided by Dr. Erik Larsson at the Department of Pathology, Uppsala University, Sweden. Sections of 5-day excisional wounds of mice were kindly provided by Dr. Sabine Werner at Max-Planck Institute for Biochemistry, Martinsried, Germany. Cryostat sections of 8 µm (unfixed, fixed in 4% paraformaldehyde, or fixed in methanol) and paraffin sections of 7 µm were washed in PBS and blocked in 3% BSA in PBS for 10 min. The sections were subsequently incubated with the following antibodies: affinity-purified sheep polyclonal antibody specific for fusion protein B (anti FP-B), which recognizes both - and ß-dystroglycan (
1-chain (
2-chain (
6-integrin subunit (
In Situ Hybridization
In situ hybridization was performed using the previously described deoxyribonucleotide probe, a 45-mer against dystroglycan mRNA (
Western Blot Analysis
Total microsomes were prepared from various adult tissues in the presence of the following protease inhibitors: aprotinin (1 µM), leupeptin (1 µM), pepstatin A (1 µM), benzamidine (1 mM), and PMSF (1 mM) (
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Results |
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ß-Dystroglycan Expression in Adult Mouse Tissues
By immunoblotting with antibody AP83 raised against ß-dystroglycan, we detected a 43-kD band representing ß-dystroglycan in all adult tissues examined (Figure 1). The lower molecular weight band at around 29 kD seen in Figure 1 (Lane 3) is a breakdown product containing the C-terminus of ß-dystroglycan. This was shown by using other C-terminal dystroglycan antibodies (data not shown).
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Expression of Dystroglycan in Skeletal Muscle
The antibodies to detect /ß-dystroglycan (anti FP-B) and ß-dystroglycan (AP83) have been described earlier (see Materials and Methods). As expected, they both stained the sarcolemmal membrane (Figure 2A and Figure 2B). In muscle, dystroglycan is also localized to the neuromuscular and myotendinous junctions (
2-chain has been described previously (
6-subunit, (
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Expression of Dystroglycan in the Digestive Tract
Salivary Gland.
Immunofluorescence analysis with anti FP-B (Figure 2E) and AP83 (Figure 2F) showed that - and ß-dystroglycan were expressed on the basal side of all epithelial cells facing the basement membranes of the adult salivary gland, including those of the interlobular ducts, serous alveoli, mucous alveoli, and mixed alveoli. In addition, the laminin
2-chain and the integrin
6-subunit were co-expressed with dystroglycan in the basement membrane regions (Figure 2G and Figure 2H). The laminin
1-chain could not be detected (data not shown).
We then analyzed dystroglycan expression in pancreas, small intestine, liver, trachea, kidney, mammary gland, testis, uterus, and skin with anti FP-B and AP83. In all tissues, except where indicated, the two antibodies gave similar results. However, only pictures of anti FP-B staining are shown.
Pancreas.
In pancreas, /ß-dystroglycan was located in the basal regions of the secretory epithelial cells. The laminin
2-chain was readily detected in the basement membrane, but the laminin
1-chain was not. The integrin
6-subunit showed a distribution similar to that of dystroglycan (data not shown).
Small Intestine.
By using anti FP-B, we found that /ß-dystroglycan was expressed in the basement membrane regions of the smooth muscle that surrounds the intestine and also in the basement membrane region of the intestinal glands. In the intestinal glands,
/ß-dystroglycan staining was also seen over the entire epithelial cell surfaces. In the villi,
/ß-dystroglycan was localized to the basement membrane area that underlies the surface epithelium. Staining was also noted in the smooth muscle located in the core of the villi (Figure 2I). By using AP83, however, we could not see any staining of ß-dystroglycan in the villi (data not shown). Polyclonal antibodies against laminin-1 stained all basement membranes, including capillary basement membranes in the small intestine (Figure 2J). The laminin
1-chain could not be detected in any basement membrane of the small intestine and the laminin
2-chain was expressed only in the basement membranes of the intestinal glands (data not shown). The integrin
6-subunit co-localized with dystroglycan in all basement membranes except those of smooth muscle (Figure 2K).
Liver.
/ß-Dystroglycan was distributed along the sinusoidal face of hepatocytes in adult liver. Laminin
1- and
2-chains were not present in the sinusoidal lining of adult mouse, because no staining could be detected with MAbs against the laminin
1- or
2-chain. On the other hand, polyclonal antibodies against laminin-1 stained the sinusoidal linings and large blood vessels, but neither the laminin
1-chain nor the laminin
2-chain could be detected in association with blood vessels (data not shown).
Expression of Dystroglycan in Trachea
In the trachea, /ß-dystroglycan was expressed in the basement membrane region of the surface epithelium as well as in the smooth muscle. The laminin
2-chain was co-expressed with dystroglycan, whereas no laminin
1-chain could be seen. Strong staining of the integrin
6-subunit was seen on the basal side of the epithelium. Both
/ß-dystroglycan and the integrin
6-subunit were detected over the entire cell surface of the surface epithelium (data not shown).
Expression of Dystroglycan in Kidney
In the embryonic kidney, expression of dystroglycan has previously been shown. Dystroglycan mRNA is produced by epithelial cells of the ureter, developing tubules, and developing glomeruli, and /ß-dystroglycan is localized at the basal side facing the basement membrane of these epithelial cells (
- and ß-dystroglycan, the strongest staining in the kidney was seen in the glomerular basement membrane.
/ß-Dystroglycan was also expressed in Bowman's capsule and in the basement membrane region of the proximal and distal tubules (Figure 2M). The polypeptides could not be detected in the basement membrane region of the collecting ducts (data not shown). Antibody AP83 reacted only with the glomerular basement membrane and not with the tubule basement membranes in adult mouse kidney (data not shown). By using FP-B antibodies on sections of adult human kidneys, a similar staining was observed as in adult mouse kidneys, i.e., staining of the glomerular basement membrane and the basement membrane region underlying proximal and distal tubule cells (Figure 2N). Antibody AP83 against ß-dystroglycan reacted only with the glomerular basement membrane in adult human kidney (data not shown).
Expression of Dystroglycan in Reproductive Organs
Mammary Gland.
Basement membranes encircling groups of breast epithelial cells showed reactivity with dystroglycan antibodies (Figure 3A). In addition, both laminin 1- and
2-chains were expressed in the basement membranes (Figure 3B and Figure 3C) as well as the integrin
6-subunit, which was localized to the basal cell surface of the epithelial cells (Figure 3D). In addition to the presence of dystroglycan in the basement membrane region, weak pericellular staining of dystroglycan was also seen in the breast epithelial cells (Figure 3A). The integrin
6-subunit was also localized pericellularly (Figure 3D).
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Testis.
In adult mouse testis, /ß-dystroglycan was confined to the basement membrane region of the seminiferous tubules (Figure 3E) where it was co-localized with laminin
1- and
2-chains (Figure 3F and Figure 3G). A peculiar pattern of the integrin
6-subunit was seen in fibroblasts dispersed close to the basement membrane (Figure 3H). Moreover, staining of dystroglycan could be noted over the entire cell surface of the seminiferous epithelium that is enclosed by the basement membrane (Figure 3E). The seminiferous epithelium consists of spermatogenic cells and the supporting Sertoli cells. It appeared that
/ß-dystroglycan was weakly expressed in the most primitive spermatogenic cells, the spermatogonia. The
6-integrin subunit, on the other hand, was expressed in the spermatozoa (Figure 3H).
Uterus. In pregnant uterus at embryonic Day 5.5, dystroglycan was prominently localized to the basement membrane of the uterine luminal epithelium (Figure 3I), uterine glandular basement membranes (Figure 3J), myoterium (Figure 3I and Figure 3J), loose connective tissue of the mesoterium (Figure 3J), large blood vessels, and some small blood vessels (Figure 3I and Figure 3J). Staining in the blood vessels appeared to be associated with smooth muscle. Dystroglycan was present as a subset of a laminin staining pattern, as shown by use of a polyclonal antibody against placental laminin (data not shown).
Expression of Dystroglycan in Skin
/ß-Dystroglycan was expressed pericellularly in all epidermal layers of the skin except for the stratum corneum (Figure 3K). This is in contrast to the integrin
6-subunit, which was present pericellularly only in the most basal cells resting on the basement membrane (Figure 3L). Weak staining of
/ß-dystroglycan could also be detected on the basal side of the cells resting on the basement membrane (Figure 3K). The integrin
6-subunit, on the other hand, was strongly expressed at the basal cell surface in contact with the basement membrane (Figure 3L). The difference in dystroglycan and integrin
6 expression was also illustrated in a 5-day mouse excisional wound. Dystroglycan was expressed pericellularly in the proliferating epidermal keratinocytes (Figure 3M), whereas the integrin
6-subunit was located pericellularly in the most basal cells and was also enriched at the basal cell surface (Figure 3N). Dystroglycan was also located over the entire cell surface, with an enrichment towards the basal side of epithelial cells in sweat glands and hair follicles (data not shown).
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Discussion |
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Dystroglycan is a novel laminin binding protein involved in muscle cell attachment to the extracellular matrix (
On the basis of our findings, dystroglycan is expressed in muscle and epithelial cells in the adult organism. In addition, dystroglycan is localized to the neuromuscular and myotendinous junctions (
Dystroglycan specifically binds the E3 fragment of the laminin 1-chain and to E3-like fragments of the laminin
2-chain (
1-chain is co-expressed with dystroglycan in the basement membranes of kidney proximal tubules, mammary gland, and testis only. The E3 fragment of laminin-1 has previously been shown to be involved in lactational differentiation of the mammary gland. A function blocking anti-
6-integrin antibody had no effect on milk protein expression, whereas ß1-integrin obviously was important for casein expression. These data suggest that either other integrin
-chains and/or other receptor types are involved in lactational differentiation (
The laminin 2-chain was co-expressed with dystroglycan in several basement membranes. These data suggest that dystroglycan might bind laminin
2 at sites where they are co-expressed. In muscle, dystroglycan and laminin
2-chain are co-expressed in the sarcolemma. An animal model for autosomal recessive muscular dystrophy is the dy mouse. Homozygous dy/dy mice have drastically reduced levels of laminin
2-chain mRNA and more than a 95% reduction of the protein. The low levels of the laminin
2-chain apparently lead to defects in the muscle basement membrane, and the mice display a dystrophic phenotype. Aside from having a progressive muscle disease these mice are smaller and die of an unknown cause between 2 and 6 months (
2-chain is also co-localized with dystroglycan in trachea, salivary gland, mammary gland, and testis. Thus far, consequences of the absence of laminin
2-chains in other organs have not been studied.
Interestingly, we could show that dystroglycan is prominently expressed in the glomerular basement membrane region of the kidney. Our results on the expression of dystroglycan in glomerular basement membrane apparently differ from previously published results (- and ß-dystroglycan and an antibody against ß-dystroglycan. Both of these reacted with the glomerular basement membrane regions in both mouse and human kidneys. The presence of dystroglycan in the glomerular basement membrane is further supported by in situ hybridization analysis showing that epithelial podocytes produce dystroglycan mRNA. Neither the laminin
1- nor the laminin
2-chain (
-chains interacting with dystroglycan. Indeed, the recently described laminin
5-chain (
1- and
2-chains. Several previous studies have suggested a more widespread distribution of the laminin
1-chain in mature tissues (
1-chain, instead detects the laminin
5-chain (
5-chain is widely distributed in mature tissues and is co-localized with dystroglycan in a number of tissues. It will now be interesting to determine whether the laminin
5-chain also binds
-dystroglycan.
The presence of /ß-dystroglycan in the tubule basement membranes of the kidney is unclear. Tubule basement membrane regions clearly reacted with anti FP-B antibodies (detecting both
- and ß-dystroglycan), whereas antibody AP83 against ß-dystroglycan failed to react with the basal side of epithelial cells of the tubules in both mouse and human kidneys. A similar observation was noted in the small intestine. Antibodies directed to both
- and ß-dystroglycan recognized the basal side of the surface epithelium of the villi. However, AP83 (against ß-dystroglycan) did not stain the basal side of the surface epithelium. These data indicate either that
-dystroglycan is present without ß-dystroglycan in the tubule basement membrane and the basement membrane region of the villi or that ß-dystroglycan is present but can not be detected because masking of the epitopes in these locations. A non-overlapping distribution of
- and ß-dystroglycan has also been shown in rat cerebellum (
-dystroglycan is present without ß-dystroglycan in certain locations.
In muscle, /ß-dystroglycan is a part of the DGC, a complex of proteins that anchors dystrophin to the sarcolemma. The major part of the other proteins in the DGC complex appears to be muscle-specific, but a few are ubiquitously expressed (
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Acknowledgments |
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Supported by grants from the Swedish Cancer Fund, Barncancerfonden, and Knut and Alice Wallenberg Stiftelsen. MDH was partially supported by the Iowa Cardiovascular Interdisciplinary Research Fellowship (HL07121) and KPC is an investigator of the Howard Hughes Medical Institute.
We thank Anne-Mari Olofsson for expert technical help.
Received for publication May 9, 1997; accepted October 30, 1997.
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