Molecular cloning of syndecan, an integral membrane proteoglycan

doi:10.1083/jcb.108.4.1547

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Molecular cloning of syndecan, an integral membrane proteoglycan

S Saunders, M Jalkanen, S O'Farrell and M Bernfield
Department of Pediatrics, Stanford University School of Medicine, California 94305.

We describe cDNA clones for a cell surface proteoglycan that bears both heparan sulfate and chondroitin sulfate and that links the cytoskeleton to the interstitial matrix. The cDNA encodes a unique core protein of 32,868 D that contains several structural features consistent with its role as a glycosamino-glycan-containing matrix anchor. The sequence shows discrete cytoplasmic, transmembrane, and NH2-terminal extracellular domains, indicating that the molecule is a type I integral membrane protein. The cytoplasmic domain is small and similar in size but not in sequence to that of the beta-chain of various integrins. The extracellular domain contains a single dibasic sequence adjacent to the extracellular face of the transmembrane domain, potentially serving as the protease-susceptible site involved in release of this domain from the cell surface. The extracellular domain contains two distinct types of putative glycosaminoglycan attachment sites; one type shows sequence characteristics of the sites previously described for chondroitin sulfate attachment (Bourdon, M. A., T. Krusius, S. Campbell, N. B. Schwartz, and E. Ruoslahti. 1987. Proc. Natl. Acad. Sci. USA. 84:3194-3198), but the other type has newly identified sequence characteristics that potentially correspond to heparan sulfate attachment sites. The single N-linked sugar recognition sequence is within the putative chondroitin sulfate attachment sequence, suggesting asparagine glycosylation as a mechanism for regulating chondroitin sulfate chain addition. Both 5' and 3' regions of this cDNA have sequences substantially identical to analogous regions of the human insulin receptor cDNA: a 99-bp region spanning the 5' untranslated and initial coding sequences is 67% identical and a 35- bp region in the 3' untranslated region is 81% identical in sequence. mRNA expression is tissue specific; various epithelial tissues show the same two sizes of mRNA (2.6 and 3.4 kb); in the same relative abundance (3:1), the cerebrum shows a single 4.5-kb mRNA. This core protein cDNA describes a new class of molecule, an integral membrane proteoglycan, that we propose to name syndecan (from the Greek syndein, to bind together).
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Lee, S.-J., Kadambi, S., David, C., Cooper, A. D., Choi, S. Y. (2004). Association of hepatic lipase with proteoglycans stimulates the production of proteoglycans in vivo and in vitro. J. Lipid Res. 45: 1266-1271 [Abstract] [Full Text]
Mulivor, A. W., Lipowsky, H. H. (2004). Inflammation- and ischemia-induced shedding of venular glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 286: H1672-H1680 [Abstract] [Full Text]
Yang, Y., Borset, M., Langford, J. K., Sanderson, R. D. (2003). Heparan Sulfate Regulates Targeting of Syndecan-1 to a Functional Domain on the Cell Surface. J. Biol. Chem. 278: 12888-12893 [Abstract] [Full Text]
Stallcup, W. B., Dahlin-Huppe, K. (2002). Chondroitin sulfate and cytoplasmic domain-dependent membrane targeting of the NG2 proteoglycan promotes retraction fiber formation and cell polarization. J. Cell Sci. 114: 2315-2325 [Abstract] [Full Text]
Rue, C. A., Ryan, P. (2002). Characterization of pseudorabies virus glycoprotein C attachment to heparan sulfate proteoglycans. J. Gen. Virol. 83: 301-309 [Abstract] [Full Text]
Monks, J., Huey, P. U., Hanson, L., Eckel, R. H., Neville, M. C., Gavigan, S. (2001). A lipoprotein-containing particle is transferred from the serum across the mammary epithelium into the milk of lactating mice. J. Lipid Res. 42: 686-696 [Abstract] [Full Text]
Adams, J. C., Kureishy, N., Taylor, A. L. (2001). A Role for Syndecan-1 in Coupling Fascin Spike Formation by Thrombospondin-1. JCB 152: 1169-1182 [Abstract] [Full Text]
Bandtlow, C. E., Zimmermann, D. R. (2000). Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins. Physiol. Rev. 80: 1267-1290 [Abstract] [Full Text]
Modrowski, D., Basle, M., Lomri, A., Marie, P. J. (2000). Syndecan-2 Is Involved in the Mitogenic Activity and Signaling of Granulocyte-Macrophage Colony-stimulating Factor in Osteoblasts. J. Biol. Chem. 275: 9178-9185 [Abstract] [Full Text]
Fitzgerald, M. L., Wang, Z., Park, P. W., Murphy, G., Bernfield, M. (2000). Shedding of Syndecan-1 and -4 Ectodomains Is Regulated by Multiple Signaling Pathways and Mediated by a Timp-3-Sensitive Metalloproteinase. JCB 148: 811-824 [Abstract] [Full Text]
Valles, S., Tsoi, C., Huang, W.-Y., Wyllie, D., Carlotti, F., Askari, J. A., Humphries, M. J., Dower, S. K., Qwarnstrom, E. E. (1999). Recruitment of a Heparan Sulfate Subunit to the Interleukin-1 Receptor Complex. REGULATION BY FIBRONECTIN ATTACHMENT. J. Biol. Chem. 274: 20103-20109 [Abstract] [Full Text]
Romaris, M., Coomans, C., Ceulemans, H., Bruystens, A.-M., Vekemans, S., David, G. (1999). Molecular Polymorphism of the Syndecans. IDENTIFICATION OF A HYPO-GLYCANATED MURINE SYNDECAN-1 SPLICE VARIANT. J. Biol. Chem. 274: 18667-18674 [Abstract] [Full Text]
Nepomuceno, R. R., Ruiz, S., Park, M., Tenner, A. J. (1999). C1qRP Is a Heavily O-Glycosylated Cell Surface Protein Involved in the Regulation of Phagocytic Activity. J. Immunol. 162: 3583-3589 [Abstract] [Full Text]
Imai, S., Kaksonen, M., Raulo, E., Kinnunen, T., Fages, C., Meng, X., Lakso, M., Rauvala, H. (1998). Osteoblast Recruitment and Bone Formation Enhanced by Cell Matrix-associated Heparin-binding Growth-associated Molecule (HB-GAM). JCB 143: 1113-1128 [Abstract] [Full Text]
Langford, J. K., Stanley, M. J., Cao, D., Sanderson, R. D. (1998). Multiple Heparan Sulfate Chains Are Required for Optimal Syndecan-1 Function. J. Biol. Chem. 273: 29965-29971 [Abstract] [Full Text]
McFall, A. J., Rapraeger, A. C. (1998). Characterization of the High Affinity Cell-binding Domain in the Cell Surface Proteoglycan Syndecan-4. J. Biol. Chem. 273: 28270-28276 [Abstract] [Full Text]
Liu, W., Litwack, E. D., Stanley, M. J., Langford, J. K., Lander, A. D., Sanderson, R. D. (1998). Heparan Sulfate Proteoglycans as Adhesive and Anti-invasive Molecules. SYNDECANS AND GLYPICAN HAVE DISTINCT FUNCTIONS. J. Biol. Chem. 273: 22825-22832 [Abstract] [Full Text]
Cohen, A. R., Wood, D. F., Marfatia, S. M., Walther, Z., Chishti, A. H., Anderson, J. M. (1998). Human CASK/LIN-2 Binds Syndecan-2 and Protein 4.1 and Localizes to the Basolateral Membrane of Epithelial Cells. JCB 142: 129-138 [Abstract] [Full Text]
Horowitz, A., Simons, M. (1998). Regulation of Syndecan-4 Phosphorylation in Vivo. J. Biol. Chem. 273: 10914-10918 [Abstract] [Full Text]
Tkachuk, M., Bolliger, S., Ryffel, B., Pluschke, G., Banks, T. A., Herren, S., Gisler, R. H., Kosco-Vilbois, M. H. (1998). Crucial Role of Tumor Necrosis Factor Receptor 1 Expression on Nonhematopoietic Cells for B Cell Localization within the Splenic White Pulp. JEM 187: 469-477 [Abstract] [Full Text]
Li, J., Brown, L. F., Laham, R. J., Volk, R., Simons, M. (1997). Macrophage-Dependent Regulation of Syndecan Gene Expression. Circ. Res. 81: 785-796 [Abstract] [Full Text]
Larrain, J., Cizmeci-Smith, G., Troncoso, V., Stahl, R. C., Carey, D. J., Brandan, E. (1997). Syndecan-1 Expression Is Down-regulated during Myoblast Terminal Differentiation. MODULATION BY GROWTH FACTORS AND RETINOIC ACID. J. Biol. Chem. 272: 18418-18424 [Abstract] [Full Text]
Subramanian, S. V., Fitzgerald, M. L., Bernfield, M. (1997). Regulated Shedding of Syndecan-1 and -4�Ectodomains by Thrombin and Growth Factor Receptor Activation. J. Biol. Chem. 272: 14713-14720 [Abstract] [Full Text]
McFall, A. J., Rapraeger, A. C. (1997). Identification of an Adhesion Site within the Syndecan-4 Extracellular Protein Domain. J. Biol. Chem. 272: 12901-12904 [Abstract] [Full Text]
Brinkmann, T., Weilke, C., Kleesiek, K. (1997). Recognition of Acceptor Proteins by UDP-D-xylose Proteoglycan Core Protein beta -D-Xylosyltransferase. J. Biol. Chem. 272: 11171-11175 [Abstract] [Full Text]
Cizmeci-Smith, G., Langan, E., Youkey, J., Showalter, L. J., Carey, D. J. (1997). Syndecan-4 Is a Primary-Response Gene Induced by Basic Fibroblast Growth Factor and Arterial Injury in Vascular Smooth Muscle Cells. Arterioscler. Thromb. Vasc. Bio. 17: 172-180 [Abstract] [Full Text]
Fernandez-Busquets, X., Kammerer, R. A., Burger, M. M. (1996). A 35-kDa Protein Is the Basic Unit of the Core from the 2�104-kDa Aggregation Factor Responsible for Species-specific Cell Adhesion in the Marine Sponge Microciona prolifera. J. Biol. Chem. 271: 23558-23565 [Abstract] [Full Text]
Kainulainen, V., Nelimarkka, L., Jarvelainen, H., Laato, M., Jalkanen, M., Elenius, K. (1996). Suppression of Syndecan-1 Expression in Endothelial Cells by Tumor Necrosis Factor-alpha. J. Biol. Chem. 271: 18759-18766 [Abstract] [Full Text]
Vihinen, T., M��tt�, A., Jaakkola, P., Auvinen, P., Jalkanen, M. (1996). Functional Characterization of Mouse Syndecan-1 Promoter. J. Biol. Chem. 271: 12532-12541 [Abstract] [Full Text]
Kojima, T., Katsumi, A., Yamazaki, T., Muramatsu, T., Nagasaka, T., Ohsumi, K., Saito, H. (1996). Human Ryudocan from Endothelium-like Cells Binds Basic Fibroblast Growth Factor, Midkine, and Tissue Factor Pathway Inhibitor. J. Biol. Chem. 271: 5914-5920 [Abstract] [Full Text]
Joseph, S., Ford, M., Barth, C, Portbury, S, Bartlett, P., Nurcombe, V, Greferath, U (1996). A proteoglycan that activates fibroblast growth factors during early neuronal development is a perlecan variant. Development 122: 3443-3452 [Abstract]
Leppa, S, Vleminckx, K, Van Roy, F, Jalkanen, M (1996). Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin-dependent. J. Cell Sci. 109: 1393-1403 [Abstract]
Schaefer, T, Roux, M, Stuhlsatz, H., Herken, R, Coulomb, B, Krieg, T, Smola, H (1996). Glycosaminoglycans modulate cell-matrix interactions of human fibroblasts and endothelial cells in vitro. J. Cell Sci. 109: 479-488 [Abstract]
Kershaw, D. B., Thomas, P. E., Wharram, B. L., Goyal, M., Wiggins, J. E., Whiteside, C. I., Wiggins, R. C. (1995). Molecular Cloning, Expression, and Characterization of Podocalyxin-like Protein 1 from Rabbit as a Transmembrane Protein of Glomerular Podocytes and Vascular Endothelium. J. Biol. Chem. 270: 29439-29446 [Abstract] [Full Text]
Watanabe, E., Maeda, N., Matsui, F., Kushima, Y., Noda, M., Oohira, A. (1995). Neuroglycan C, a Novel Membrane-spanning Chondroitin Sulfate Proteoglycan That Is Restricted to the Brain. J. Biol. Chem. 270: 26876-26882 [Abstract] [Full Text]
Zhang, L., David, G., Esko, J. D. (1995). Repetitive Ser-Gly Sequences Enhance Heparan Sulfate Assembly in Proteoglycans. J. Biol. Chem. 270: 27127-27135 [Abstract] [Full Text]
Inoue, S (1995). Possible continuity of subplasmalemmal cytoplasmic network with basement membrane cord network: ultrastructural study. J. Cell Sci. 108: 1971-1976 [Abstract]
Mitsiadis, T., Salmivirta, M, Muramatsu, T, Muramatsu, H, Rauvala, H, Lehtonen, E, Jalkanen, M, Thesleff, I (1995). Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121: 37-51 [Abstract]
Elenius, K, Jalkanen, M (1994). Function of the syndecans--a family of cell surface proteoglycans. J. Cell Sci. 107: 2975-2982
Quarto, N, Amalric, F (1994). Heparan sulfate proteoglycans as transducers of FGF-2 signalling. J. Cell Sci. 107: 3201-3212 [Abstract]
Miettinen, H., Jalkanen, M (1994). The cytoplasmic domain of syndecan-1 is not required for association with Triton X-100-insoluble material. J. Cell Sci. 107: 1571-1581 [Abstract]
Bertolami, C. N., Messadi, D. V. (1994). The Role of Proteoglycans in Hard and Soft Tissue Repair. CROBM 5: 311-337 [Abstract] [Full Text]
David, G., Bai, X. M., Van der Schueren, B., Marynen, P., Cassiman, J. J., Van den Berghe, H. (1993). Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development 119: 841-854 [Abstract]
Kan, M, Wang, F, Xu, J, Crabb, J., Hou, J, McKeehan, W. (1993). An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259: 1918-1921 [Abstract]
Wu, X., Sun, T. (1993). Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein. J. Cell Sci. 106: 31-43 [Abstract]
Ruoslahti, E., Yamaguchi, Y., Hildebrand, A., Border, W.A. (1992). Extracellular Matrix/Growth Factor Interactions. Cold Spring Harb Symp Quant Biol 57: 309-315 [Abstract]
Rahemtulla, F. (1992). Proteoglycans of Oral Tissues. CROBM 3: 135-162 [Full Text]
Rapraeger, A., Krufka, A, Olwin, B. (1991). Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252: 1705-1708 [Abstract]
Cutler, L. S., Gremski, W. (1991). Epithelial-Mesenchymal Interactions in the Development of Salivary Glands. CROBM 2: 1-12 [Abstract] [Full Text]
Uitto, V.-J., Larjava, H. (1991). Extracellular Matrix Molecules and their Receptors: An Overview with Special Emphasis on Periodontal Tissues. CROBM 2: 323-354 [Abstract] [Full Text]
Reichardt, L.F., Bossy, B., Carbonetto, S., de Curtis, I., Emmett, C., Hall, D.E., Ignatius, M.J., Lefcort, F., Napolitano, E., Large, T., Neugebauer, K.M., Tomaselli, K.J. (1990). Neuronal Receptors That Regulate Axon Growth. Cold Spring Harb Symp Quant Biol 55: 341-350 [Abstract]
Renne, T., Dedio, J., David, G., Muller-Esterl, W. (2000). High Molecular Weight Kininogen Utilizes Heparan Sulfate Proteoglycans for Accumulation on Endothelial Cells. J. Biol. Chem. 275: 33688-33696 [Abstract] [Full Text]