Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan

A cDNA clone coding for a membrane proteoglycan core protein was isolated from a neonatal rat Schwann cell cDNA library by screening with an oligonucleotide based on a conserved sequence in cDNAs coding for previously described proteoglycan core proteins. Primer extension and polymerase chain reaction amplification were used to obtain additional 5' protein coding sequences. The deduced amino acid sequence predicted a 353 amino acid polypeptide with a single membrane spanning segment and a 34 amino acid hydrophilic COOH-terminal cytoplasmic domain. The putative extracellular domain contains three potential glycosaminoglycan attachment sites, as well as a domain rich in Thr and Pro residues. Analysis of the cDNA and deduced amino acid sequences revealed a high degree of identity with the transmembrane and cytoplasmic domains of previously described proteoglycans but a unique extracellular domain sequence. On Northern blots the cDNA hybridized to a single 5.6-kb mRNA that was present in Schwann cells, neonatal rat brain, rat heart, and rat smooth muscle cells. A 16-kD protein fragment encoded by the cDNA was expressed in bacteria and used to immunize rabbits. The resulting antibodies reacted on immunoblots with the core protein of a detergent extracted heparan sulfate proteoglycan. The core protein had an apparent mass of 120 kD. When the anti-core protein antibodies were used to stain tissue sections immunoreactivity was present in peripheral nerve, newborn rat brain, heart, aorta, and other neonatal tissues. A ribonuclease protection assay was used to quantitate levels of the core protein mRNA. High levels were found in neonatal rat brain, heart, and Schwann cells. The mRNA was barely detectable in neonatal or adult liver, or adult brain.

[1]  M. Laato,et al.  Induced expression of syndecan in healing wounds , 1991, The Journal of cell biology.

[2]  B. Olwin,et al.  Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation , 1991, Science.

[3]  J. Schwarzbauer,et al.  Localization of the major heparin-binding site in fibronectin. , 1991, The Journal of biological chemistry.

[4]  Jeffrey D. Esko,et al.  Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor , 1991, Cell.

[5]  P. Marynen,et al.  Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts , 1990, The Journal of cell biology.

[6]  D. Carey,et al.  Association of cell surface heparan sulfate proteoglycans of Schwann cells with extracellular matrix proteins. , 1990, The Journal of biological chemistry.

[7]  D. Carey,et al.  Identification of a lipid-anchored heparan sulfate proteoglycan in Schwann cells , 1990, The Journal of cell biology.

[8]  M. Salmivirta,et al.  Binding of human syndecan to extracellular matrix proteins. , 1990, The Journal of biological chemistry.

[9]  W. Wagner,et al.  Characterization of extracellular matrix proteoglycan transcripts expressed by vascular smooth muscle cells. , 1990, European journal of cell biology.

[10]  P. Jaakkola,et al.  Sequence of human syndecan indicates a novel gene family of integral membrane proteoglycans. , 1990, The Journal of biological chemistry.

[11]  R. Sanderson,et al.  B lymphocytes express and lose syndecan at specific stages of differentiation. , 1989, Cell regulation.

[12]  E. Tsilibary,et al.  Mapping of three major heparin-binding sites on laminin and identification of a novel heparin-binding site on the B1 chain. , 1989, The Journal of biological chemistry.

[13]  I. Thesleff,et al.  Syndecan from embryonic tooth mesenchyme binds tenascin. , 1989, The Journal of biological chemistry.

[14]  D. Rifkin,et al.  Recent developments in the cell biology of basic fibroblast growth factor , 1989, The Journal of cell biology.

[15]  D. Carey,et al.  Inhibition of proteoglycan synthesis alters extracellular matrix deposition, proliferation, and cytoskeletal organization of rat aortic smooth muscle cells in culture , 1989, The Journal of cell biology.

[16]  I. Thesleff,et al.  Syndecan and tenascin expression is induced by epithelial-mesenchymal interactions in embryonic tooth mesenchyme , 1989, The Journal of cell biology.

[17]  G. J. Cole,et al.  Characterization of a heparan sulfate proteoglycan that copurifies with the neural cell adhesion molecule. , 1989, Experimental cell research.

[18]  D. Carey,et al.  Membrane anchoring of heparan sulfate proteoglycans by phosphatidylinositol and kinetics of synthesis of peripheral and detergent-solubilized proteoglycans in Schwann cells , 1989, The Journal of cell biology.

[19]  P. Marynen,et al.  Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. Prediction of an integral membrane domain and evidence for multiple distinct core proteins at the cell surface of human lung fibroblasts. , 1989, The Journal of biological chemistry.

[20]  M. Jalkanen,et al.  Molecular cloning of syndecan, an integral membrane proteoglycan , 1989, The Journal of cell biology.

[21]  M. Kozak The scanning model for translation: an update , 1989, The Journal of cell biology.

[22]  M. Bernfield,et al.  Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix , 1988, The Journal of cell biology.

[23]  J. Gibrat,et al.  Further developments of protein secondary structure prediction using information theory. New parameters and consideration of residue pairs. , 1987, Journal of molecular biology.

[24]  M. Jalkanen,et al.  Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study. , 1987, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[25]  W. Frazier Thrombospondin: a modular adhesive glycoprotein of platelets and nucleated cells , 1987, The Journal of cell biology.

[26]  J. Herz,et al.  Efficient construction of cDNA libraries in plasmid expression vectors using an adaptor strategy. , 1986, Nucleic acids research.

[27]  L. Glaser,et al.  Cell-substratum adhesion in chick neural retina depends upon protein- heparan sulfate interactions , 1985, The Journal of cell biology.

[28]  J. Uitto,et al.  Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation , 1980, The Journal of cell biology.

[29]  J. Shively,et al.  Formation of anhydrosugars in the chemical depolymerization of heparin. , 1976, Biochemistry.

[30]  Z. Fuks,et al.  Extracellular sequestration and release of fibroblast growth factor: a regulatory mechanism? , 1991, Trends in biochemical sciences.

[31]  L. Kjellén,et al.  Proteoglycans: structures and interactions. , 1991, Annual review of biochemistry.

[32]  L. Fransson Structure and function of cell-associated proteoglycans , 1987 .