Non-muscle alpha-dystroglycan is involved in epithelial development

doi:10.1083/jcb.130.1.79

This Article

	Full Text (PDF, 11851K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Durbeej, M.
	Articles by Ekblom, P.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Durbeej, M.
	Articles by Ekblom, P.


Social Bookmarking

	What's this?

ARTICLES

Non-muscle alpha-dystroglycan is involved in epithelial development

M Durbeej, E Larsson, O Ibraghimov-Beskrovnaya, SL Roberds, KP Campbell and P Ekblom
Department of Animal Physiology, Uppsala University, Sweden.

The dystroglycan complex is a transmembrane linkage between the cytoskeleton and the basement membrane in muscle. One of the components of the complex, alpha-dystroglycan binds both laminin of muscle (laminin-2) and agrin of muscle basement membranes. Dystroglycan has been detected in nonmuscle tissues as well, but the physiological role in nonmuscle tissues has remained unknown. Here we show that dystroglycan during mouse development in nonmuscle tissues is expressed in epithelium. In situ hybridization revealed strong expression of dystroglycan mRNA in all studied epithelial sheets, but not in endothelium or mesenchyme. Conversion of mesenchyme to epithelium occurs during kidney development, and the embryonic kidney was used to study the role of alpha-dystroglycan for epithelial differentiation. During in vitro culture of the metanephric mesenchyme, the first morphological signs of epithelial differentiation can be seen on day two. Northern blots revealed a clear increase in dystroglycan mRNA on day two of in vitro development. A similar increase of expression on day two was previously shown for laminin alpha 1 chain. Immunofluorescence showed that dystroglycan is strictly located on the basal side of developing kidney epithelial cells. Monoclonal antibodies known to block binding of alpha-dystroglycan to laminin-1 perturbed development of epithelium in kidney organ culture, whereas control antibodies did not do so. We suggest that the dystroglycan complex acts as a receptor for basement membrane components during epithelial morphogenesis. It is likely that this involves binding of alpha- dystroglycan to E3 fragment of laminin-1.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Lommel, M., Strahl, S. (2009). Protein O-mannosylation: Conserved from bacteria to humans. Glycobiology 19: 816-828 [Abstract] [Full Text]
Masuda-Hirata, M., Suzuki, A., Amano, Y., Yamashita, K., Ide, M., Yamanaka, T., Sakai, M., Imamura, M., Ohno, S. (2009). Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. GENES CELLS 14: 835-850 [Abstract] [Full Text]
de Bernabe, D. B.-V., Inamori, K.-i., Yoshida-Moriguchi, T., Weydert, C. J., Harper, H. A., Willer, T., Henry, M. D., Campbell, K. P. (2009). Loss of {alpha}-Dystroglycan Laminin Binding in Epithelium-derived Cancers Is Caused by Silencing of LARGE. J. Biol. Chem. 284: 11279-11284 [Abstract] [Full Text]
Gong, Y., Zhang, R., Zhang, J., Xu, L., Zhang, F., Xu, W., Wang, Y., Chu, Y., Xiong, S. (2008). {alpha}-Dystroglycan is involved in positive selection of thymocytes by participating in immunological synapse formation. FASEB J. 22: 1426-1439 [Abstract] [Full Text]
Watanabe, N., Sasaoka, T., Noguchi, S., Nishino, I., Tanaka, T. (2007). Cys669-Cys713 disulfide bridge formation is a key to dystroglycan cleavage and subunit association.. GENES CELLS 12: 75-88 [Abstract] [Full Text]
Weir, M. L., Oppizzi, M. L., Henry, M. D., Onishi, A., Campbell, K. P., Bissell, M. J., Muschler, J. L. (2006). Dystroglycan loss disrupts polarity and {beta}-casein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119: 4047-4058 [Abstract] [Full Text]
Driss, A., Charrier, L., Yan, Y., Nduati, V., Sitaraman, S., Merlin, D. (2006). Dystroglycan receptor is involved in integrin activation in intestinal epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G1228-G1242 [Abstract] [Full Text]
Johnson, R. P., Kang, S. H., Kramer, J. M. (2006). C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin. Development 133: 1911-1921 [Abstract] [Full Text]
Barresi, R., Campbell, K. P. (2006). Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119: 199-207 [Abstract] [Full Text]
Vogtlander, N. P.J., Dijkman, H., Bakker, M. A.H., Campbell, K. P., van der Vlag, J., Berden, J. H.M. (2005). Localization of {alpha}-Dystroglycan on the Podocyte: from Top to Toe. J. Histochem. Cytochem. 53: 1345-1353 [Abstract] [Full Text]
Singh, J., Itahana, Y., Knight-Krajewski, S., Kanagawa, M., Campbell, K. P., Bissell, M. J., Muschler, J. (2004). Proteolytic Enzymes and Altered Glycosylation Modulate Dystroglycan Function in Carcinoma Cells. Cancer Res. 64: 6152-6159 [Abstract] [Full Text]
Spence, H.J., Chen, Y.-J., Batchelor, C.L., Higginson, J.R., Suila, H., Carpen, O., Winder, S.J. (2004). Ezrin-dependent regulation of the actin cytoskeleton by {beta}-dystroglycan. Hum Mol Genet 13: 1657-1668 [Abstract] [Full Text]
Kanwar, Y. S., Wada, J., Lin, S., Danesh, F. R., Chugh, S. S., Yang, Q., Banerjee, T., Lomasney, J. W. (2004). Update of extracellular matrix, its receptors, and cell adhesion molecules in mammalian nephrogenesis. Am. J. Physiol. Renal Physiol. 286: F202-F215 [Abstract] [Full Text]
Brown, S. C., Torelli, S., Brockington, M., Yuva, Y., Jimenez, C., Feng, L., Anderson, L., Ugo, I., Kroger, S., Bushby, K., Voit, T., Sewry, C., Muntoni, F. (2004). Abnormalities in {alpha}-Dystroglycan Expression in MDC1C and LGMD2I Muscular Dystrophies. Am. J. Pathol. 164: 727-737 [Abstract] [Full Text]
Grewal, P. K., Hewitt, J. E. (2003). Glycosylation defects: a new mechanism for muscular dystrophy?. Hum Mol Genet 12: R259-264 [Abstract] [Full Text]
Ferletta, M., Kikkawa, Y., Yu, H., Talts, J. F., Durbeej, M., Sonnenberg, A., Timpl, R., Campbell, K. P., Ekblom, P., Genersch, E. (2003). Opposing Roles of Integrin {alpha}6A{beta}1 and Dystroglycan in Laminin-mediated Extracellular Signal-regulated Kinase Activation. Mol. Biol. Cell 14: 2088-2103 [Abstract] [Full Text]
Deng, W.-M., Schneider, M., Frock, R., Castillejo-Lopez, C., Gaman, E. A., Baumgartner, S., Ruohola-Baker, H. (2003). Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130: 173-184 [Abstract] [Full Text]
Muschler, J., Levy, D., Boudreau, R., Henry, M., Campbell, K., Bissell, M. J. (2002). A Role for Dystroglycan in Epithelial Polarization: Loss of Function in Breast Tumor Cells. Cancer Res. 62: 7102-7109 [Abstract] [Full Text]
Collins, B. J., Gorelick, G., Schneider, A. B. (2001). Dystroglycan Is Present in Rat Thyroid and Rat Thyroid Cells and Responds to Thyrotropin. Endocrinology 142: 3152-3162 [Abstract] [Full Text]
Li, X., Chen, Y., Scheele, S., Arman, E., Haffner-Krausz, R., Ekblom, P., Lonai, P. (2001). Fibroblast Growth Factor Signaling and Basement Membrane Assembly Are Connected during Epithelial Morphogenesis of the Embryoid Body. JCB 153: 811-822 [Abstract] [Full Text]
White, S. R., Wojcik, K. R., Gruenert, D., Sun, S., Dorscheid, D. R. (2001). Airway Epithelial Cell Wound Repair Mediated by {alpha}-Dystroglycan. Am. J. Respir. Cell Mol. Bio. 24: 179-186 [Abstract] [Full Text]
Henry, M., Satz, J., Brakebusch, C, Costell, M, Gustafsson, E, Fassler, R, Campbell, K. (2001). Distinct roles for dystroglycan, (&bgr;)1 integrin and perlecan in cell surface laminin organization. J. Cell Sci. 114: 1137-1144 [Abstract]
Raats, C. J. I., van den Born, J., Bakker, M. A. H., Oppers-Walgreen, B., Pisa, B. J. M., Dijkman, H. B. P. M., Assmann, K. J. M., Berden, J. H. M. (2000). Expression of Agrin, Dystroglycan, and Utrophin in Normal Renal Tissue and in Experimental Glomerulopathies. Am. J. Pathol. 156: 1749-1765 [Abstract] [Full Text]
REGELE, H. M., FILLIPOVIC, E., LANGER, B., POCZEWKI, H., KRAXBERGER, I., BITTNER, R. E., KERJASCHKI, D. (2000). Glomerular Expression of Dystroglycans Is Reduced in Minimal Change Nephrosis But Not in Focal Segmental Glomerulosclerosis. J. Am. Soc. Nephrol. 11: 403-412 [Abstract] [Full Text]
Loh, N., Newey, S., Davies, K., Blake, D. (2000). Assembly of multiple dystrobrevin-containing complexes in the kidney. J. Cell Sci. 113: 2715-2724 [Abstract]
James, M, Nuttall, A, Ilsley, J., Ottersbach, K, Tinsley, J., Sudol, M, Winder, S. (2000). Adhesion-dependent tyrosine phosphorylation of (beta)-dystroglycan regulates its interaction with utrophin. J. Cell Sci. 113: 1717-1726 [Abstract]
Durbeej, M., Campbell, K. P. (1999). Biochemical Characterization of the Epithelial Dystroglycan Complex. J. Biol. Chem. 274: 26609-26616 [Abstract] [Full Text]
Muschler, J., Lochter, A., Roskelley, C. D., Yurchenco, P., Bissell, M. J. (1999). Division of Labor among the alpha 6beta 4 Integrin, beta 1 Integrins, and an E3 Laminin Receptor to Signal Morphogenesis and beta -Casein Expression in Mammary Epithelial Cells. Mol. Biol. Cell 10: 2817-2828 [Abstract] [Full Text]
Montanaro, F., Lindenbaum, M., Carbonetto, S. (1999). {alpha}-Dystroglycan Is a Laminin Receptor Involved in Extracellular Matrix Assembly on Myotubes and Muscle Cell Viability. JCB 145: 1325-1340 [Abstract] [Full Text]
Shimizu, H., Hosokawa, H., Ninomiya, H., Miner, J. H., Masaki, T. (1999). Adhesion of Cultured Bovine Aortic Endothelial Cells to Laminin-1 Mediated by Dystroglycan. J. Biol. Chem. 274: 11995-12000 [Abstract] [Full Text]
Kachinsky, A. M., Froehner, S. C., Milgram, S. L. (1999). A PDZ-containing Scaffold Related to the Dystrophin Complex at the Basolateral Membrane of Epithelial Cells. JCB 145: 391-402 [Abstract] [Full Text]
Muller, U, Brandli, A. (1999). Cell adhesion molecules and extracellular-matrix constituents in kidney development and disease. J. Cell Sci. 112: 3855-3867 [Abstract]
Ferletta, M, Ekblom, P (1999). Identification of laminin-10/11 as a strong cell adhesive complex for a normal and a malignant human epithelial cell line. J. Cell Sci. 112: 1-10 [Abstract]
Brown, S., Fassati, A, Popplewell, L, Page, A., Henry, M., Campbell, K., Dickson, G (1999). Dystrophic phenotype induced in vitro by antibody blockade of muscle alpha-dystroglycan-laminin interaction. J. Cell Sci. 112: 209-216 [Abstract]
Rambukkana, A., Yamada, H., Zanazzi, G., Mathus, T., Salzer, J. L., Yurchenco, P. D., Campbell, K. P., Fischetti, V. A. (1998). Role of -Dystroglycan as a Schwann Cell Receptor for Mycobacterium leprae. Science 282: 2076-2079 [Abstract] [Full Text]
Wallner, E. I., Yang, Q., Peterson, D. R., Wada, J., Kanwar, Y. S. (1998). Relevance of extracellular matrix, its receptors, and cell adhesion molecules in mammalian nephrogenesis. Am. J. Physiol. Renal Physiol. 275: F467-F477 [Abstract] [Full Text]
Smalheiser, N. R., Haslam, S. M., Sutton-Smith, M., Morris, H. R., Dell, A. (1998). Structural Analysis of Sequences O-Linked to Mannose Reveals a Novel Lewis X Structure in Cranin (Dystroglycan) Purified from Sheep Brain. J. Biol. Chem. 273: 23698-23703 [Abstract] [Full Text]
Raats, C. J.�I., Bakker, M. A.�H., Hoch, W., Tamboer, W. P.�M., Groffen, A. J.�A., van den Heuvel, L. P.�W.�J., Berden, J. H.�M., van den Born, J. (1998). Differential Expression of Agrin in Renal Basement Membranes As Revealed by Domain-specific Antibodies. J. Biol. Chem. 273: 17832-17838 [Abstract] [Full Text]
Durbeej, M., Henry, M. D., Ferletta, M., Campbell, K. P., Ekblom, P. (1998). Distribution of Dystroglycan in Normal Adult Mouse Tissues. J. Histochem. Cytochem. 46: 449-458 [Abstract] [Full Text]
Ueda, H., Gohdo, T., Ohno, S. (1998). b-Dystroglycan Localization in the Photoreceptor and Muller cells in the Rat Retina Revealed by Immunoelectron Microscopy. J. Histochem. Cytochem. 46: 185-192 [Abstract] [Full Text]
Gesemann, M., Brancaccio, A., Schumacher, B., Ruegg, M. A. (1998). Agrin Is a High-affinity Binding Protein of Dystroglycan in Non-muscle Tissue. J. Biol. Chem. 273: 600-605 [Abstract] [Full Text]
Groffen, A. J., Ruegg, M. A., Dijkman, H., van de Velden, T. J., Buskens, C. A., van den Born, J., Assmann, K. J., Monnens, L. A., Veerkamp, J. H., van den Heuvel, L. P. (1998). Agrin Is a Major Heparan Sulfate Proteoglycan in the Human Glomerular Basement Membrane. J. Histochem. Cytochem. 46: 19-28 [Abstract] [Full Text]
Ettinger, A. J., Feng, G., Sanes, J. R. (1997). epsilon -Sarcoglycan, a Broadly Expressed Homologue of the Gene Mutated in Limb-Girdle Muscular Dystrophy 2D. J. Biol. Chem. 272: 32534-32538 [Abstract] [Full Text]
Ervasti, J. M., Burwell, A. L., Geissler, A. L. (1997). Tissue-specific Heterogeneity in alpha -Dystroglycan Sialoglycosylation. SKELETAL MUSCLE alpha -DYSTROGLYCAN IS A LATENT RECEPTOR FOR VICIA VILLOSA AGGLUTININ B4 MASKED BY SIALIC ACID MODIFICATION. J. Biol. Chem. 272: 22315-22321 [Abstract] [Full Text]
Matsumura, K., Chiba, A., Yamada, H., Fukuta-Ohi, H., Fujita, S., Endo, T., Kobata, A., Anderson, L. V.�B., Kanazawa, I., Campbell, K. P., Shimizu, T. (1997). A Role of Dystroglycan in Schwannoma Cell Adhesion to Laminin. J. Biol. Chem. 272: 13904-13910 [Abstract] [Full Text]
Grady, R. M., Merlie, J. P., Sanes, J. R. (1997). Subtle Neuromuscular Defects in Utrophin-deficient Mice. JCB 136: 871-882 [Abstract] [Full Text]
Kadoya, Y, Salmivirta, K, Talts, J., Kadoya, K, Mayer, U, Timpl, R, Ekblom, P (1997). Importance of nidogen binding to laminin gamma1 for branching epithelial morphogenesis of the submandibular gland. Development 124: 683-691 [Abstract]
Echtermeyer, F., Sch�ber, S., P�schl, E., von der Mark, H., von der Mark, K. (1996). Specific Induction of Cell Motility on Laminin by alpha7 Integrin. J. Biol. Chem. 271: 2071-2075 [Abstract] [Full Text]
Falk, M, Salmivirta, K, Durbeej, M, Larsson, E, Ekblom, M, Vestweber, D, Ekblom, P (1996). Integrin alpha 6B beta 1 is involved in kidney tubulogenesis in vitro. J. Cell Sci. 109: 2801-2810 [Abstract]
Kanwar, Y. S., Kumar, A., Ota, K., Lin, S., Wada, J., Chugh, S., Wallner, E. I. (2002). Identification of developmentally regulated mesodermal-specific transcript in mouse embryonic metanephros. Am. J. Physiol. Renal Physiol. 282: F953-F965 [Abstract] [Full Text]