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Tissue variation of two large chondroitin sulfate proteoglycans (PG-M/versican and PG-H/aggrecan) in chick embryos

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Abstract

PG-M and PG-H, chick large chondroitin sulfate proteoglycans corresponding to versican (fibroblasttype proteoglycan) and aggrecan (cartilage-characteristic proteoglycan), respectively, which are found in mammals, have been characterized in various tissues of chick embryos. Their distribution and the compositions of the core molecules were analyzed by immunofluorescence staining and immunoblotting, respectively, using various monospecific antibodies. Molecules reactive to a monoclonal antibody to the PG-M core protein (designated MY-174) were distributed in various tissues, including aorta, lung, cornea, brain, skeletal muscle and dermis. Immunoblotting with MY-174 of the chondroitinase ABC-digested tissue extracts showed a tissue variation of MY-174-reactive core molecules (550-kD, 500-kD, 450kD, and 350-300-kD). In contrast, PG-H, besides massive occurrence in cartilage, was only found in a few tissues such as aorta and brain. In addition, PG-H in aorta, cornea, and skin was atypical in structure, because it lacked keratan sulfate. The expression of PG-M in developing chick embryos was then examined. PG-M was found in some developmentally active areas, such as the perinotochordal mesenchyme between notochord and neural tube, the basement membranes facing neuroepithelial cells, and condensing mesenchymal cells in limb buds, suggesting some functions distinctive of the developing tissues.

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References

  • Chiquet M, Fambrough DM (1984) Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked submits. J Cell Biol 98:1937–1946

    Google Scholar 

  • Doege K, Sasaki M, Horigan E, Hassell JR, Yamada Y (1987) Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J Biol Chem 262:17757–17767

    Google Scholar 

  • Edelman GM (1986) Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol 2:81–116

    Google Scholar 

  • Fisher LW, Termine JD, Young MF (1989) Deduced protein sequence of bone small proteoglycan I (biglycan) shows homology with proteoglycan II (decorin) and several nonconnective tissue proteins in a variety of species. J Biol Chem 264:4571–4576

    Google Scholar 

  • Funderburgh JL (1990) Isoforms of corneal keratan sulfate proteoglycan. J Biol Chem 265:8297–8303

    Google Scholar 

  • Gallagher JT (1989) The extended family of proteoglycans: social residents of the pericellular zone. Curr Op Cell Biol 1:1201–1218

    Google Scholar 

  • Gowda DC, Margolis RU, Margolis RK (1989) Presence of the HNK-1 epitope on poly (N-acetyllactosaminyl) oligosaccharides and identification of multiple core proteins in the chondroitin sulfate proteoglycans of brain. Biochemistry 28:4468–4474

    Google Scholar 

  • Habuchi H, Kimata K, Suzuki S (1986) Changes in proteoglycan composition during development of rat skin. J Biol Chem 261:1031–1040

    Google Scholar 

  • Hassell JR, Kimura JH, Hascall VC (1986) Proteoglycan core protein families. Annu Rev Biochem 55:539–567

    Google Scholar 

  • Heinegard D, Bjorne-Persson A, Coster L, Franzen A, Gardell S, Malmstrom A, Paulsson M, Sandfalk R, Vogel K (1985) The core proteins of large and small interstitial proteoglycans from various connective tissues from distinct subgroups. Biochem J 230:181–194

    Google Scholar 

  • Hoffman S, Crossin KL, Edelman GM (1988) Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J Cell Biol 106:519–532

    Google Scholar 

  • Kessler SW (1975) Rapid isolation of antigens from cells with a Staphylococcal protein A-antibody adsorbent: parameters of the isolation of antibody-antigen complexes with protein A. J Immunol 115:1617–1624

    Google Scholar 

  • Kimata K, Oike Y, Ito K, Karasawa K, Suzuki S (1978) The occurrence of low buoyant density proteoglycans in embryonic chick cartilage. Biochem Biophys Res Commun 85:1431–1439

    Google Scholar 

  • Kimata K, Oike Y, Tani K, Shinomura T, Yamagata M, Uritani M, Suzuki S (1986) A large chondroitin sulfate proteoglycan (PG-M) synthesized before chondrogenesis in the limb bud of chick embryo. J Biol Chem 261:13517–13525

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  • Lark MW, Yeo TK, Mar H, Lara S, Hellstrom I, Hellstrom KE, Wight TN (1987) Arterial chondroitin sulfate proteoglycan: Location with a monoclonal antibody. J Histochem Cytochem 36:1211–1221

    Google Scholar 

  • Lumsden A (1991) Motorizing the spinal cord. Cell 64:471–473

    Google Scholar 

  • Mangkornkanok-Mark M, Eisenstein R, Bahu MR (1981) Immunologic studies of bovine aortic and cartilage proteoglycans. J Histochem Cytochem 29:547–552

    Google Scholar 

  • Merril CR, Switzer RC, Van Keuren ML (1979) Trace polypeptides in cellular extracts and human body fluids detected by twodimensional electrophoresis and a highly sensitive silver stain. Proc Natl Acad Sci USA 76:4335–4339

    Google Scholar 

  • Midura RJ, Hascall VC (1989) Analysis of the proteoglycans synthesized by corneal explants from embryonic chicken. J Biol Chem 264:1423–1430

    Google Scholar 

  • Morita H, Takeuchi T, Suzuki S, Maeda K, Yamada K, Eguchi G, Kimata K (1990) Aortic endothelial cells synthesize a large chondroitin sulphate proteoglycan capable of binding to hyaluronate. Biochem J 265:61–68

    Google Scholar 

  • Nakazawa K, Hassell JR, Hascall VC, Newsome DA (1983) Heterogeneity of proteoglycans in monkey cornea stroma. Arch Biochem Biophys 222:105–116

    Google Scholar 

  • Noro A, Kimata K, Oike Y, Shinomura T, Maeda N, Yano S, Takahashi N, Suzuki S (1983) Isolation and characterization of a third proteoglycan (PG-Lt) from chick embryo cartilage which contains disulfide-bonded collagenous polypeptide. J Biol Chem 258:9323–9331

    Google Scholar 

  • Oettinger HF, Tahl G, Sasse J, Holtzer H, Pacific M (1985) Immunological analysis of chick notochord and cartilage matrix development with antisera to cartilage matrix macromolecules. Dev Biol 109:63–71

    Google Scholar 

  • Oike Y, Kimata K, Shinomura T, Nakazawa K, Suzuki S (1980) Structural analysis of chick-embryo cartilage proteoglycan by selective degradation with chondroitin lyases (Chondroitinases) and endo-b-d-galactosidase (keratanase). Biochem J 191:193–207

    Google Scholar 

  • Oldberg A, Antonsson P, Lindblom K, Heinegard D (1989) A collagen-binding 59-kD protein (fibromodulin) is structurally related to the small interstitial proteoglycans PG-S1 and PG-S2 (decorin). EMBO J 8:2601–2604

    Google Scholar 

  • Oohira A, Matsui F, Matsuda T, Takida Y, Kuboki Y (1988) Occurrence of three distinct molecular species of chondroitin sulfate proteoglycan in the developing rat brain. J Biol Chem 263:10240–10246

    Google Scholar 

  • Pechak DG, Carrino AD, Caplan IA (1985) Electron microscopic characterization of chick embryonic skeletal muscle proteoglycans. J Cell Biol 100:1767–1776

    Google Scholar 

  • Plaas AHK, Ison AL, Ackland J (1989) Synthesis of small proteoglycans substituted with keratan sulfate by rabbit articular chondrocytes. J Biol Chem 264:14447–14454

    Google Scholar 

  • Radhakrishnamurthy B, Smart F, Dalferes ER Jr, Berenson GS (1980) Isolation and characterization of proteoglycans from bovine lung. J Biol Chem 255:7575–7582

    Google Scholar 

  • Ruoslahti E (1989) Proteoglycans in cell regulation. J Biol Chem 264:13369–13372

    Google Scholar 

  • Shinomura T, Kimata K, Oike Y, Noro A, Hirose N, Tanabe K, Suzuki S (1983) The occurrence of three proteoglycan species in chick embryo cartilage. J Biol Chem 258:9314–9322

    Google Scholar 

  • Shinomura T, Kimata K, Oike Y, Maeda N, Yano S, Suzuki S (1984) Appearance of distinct types of proteoglycan in a welldefined temporal and spatial pattern during early cartilage formation in the chick limb. Dev Biol 103:211–220

    Google Scholar 

  • Shinomura T, Jensen KL, Yamagata M, Kimata K, Solursh M (1990) The distribution of mesenchyme proteoglycan (PG-M) during wing bud outgrowth. Anat Embryol 181:227–233

    Google Scholar 

  • Shinomura T, Kimata K (1992) Proteoglycan-Lb. a small dermatan sulfate proteoglycan expressed in embryonic chick epiphyseal cartilage, is structurally related to osteoinductive factor. J Biol Chem 267:1265–1270

    Google Scholar 

  • Shinomura T, Nishida Y, Kimata K (1992) A large chondroitin sulfate proteoglycan (PG-M) and cartilage differentiation. In: Kuettner et al. (eds) Articular cartilage and osteoarthritis. Raven Press, New York, pp 35–45

    Google Scholar 

  • Soledad Fernandez M, Dennis JE, Drushel RF, Carrino DA, Kimata K, Yamagata M, Caplan AI (1991) The dynamics of compartmentalization of embryonic muscle by extracellular matrix molecules. Dev Biol 147:46–61

    Google Scholar 

  • Takeda M, Iwata H, Suzuki S, Brown KS, Kimata K (1986) Correction of abnormal matrix formed by cmd/cmd chondrocytes in culture by exogenously added cartilage proteoglycan. J Cell Biol 103:1605–1614

    Google Scholar 

  • Tan S-S, Crossin KL, Hoffman S, Edelman GM (1987) Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc Natl Acad Sci USA 84:7977–7981

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    CAS  PubMed  Google Scholar 

  • Tsukahara T, Okamura M, Suzuki S, Iwata H, Miura T, Kimata K (1991) Enhanced expression of fibronectin by cmd/cmd chondrocytes and its modulation by exogenously added proteoglycan. J Cell Sci 100:387–395

    Google Scholar 

  • Vaughan L, Winterhalter KH, Bruckner P (1985) Proteoglycan Lt from chicken embryo sternum identified as type IX collagen. J Biol Chem 260:4758–4763

    Google Scholar 

  • Vogel KG, Heinegard D (1985) Characterization of proteoglycans from adult bovine tendon. J Biol Chem 260:9298–9306

    Google Scholar 

  • Wight TN, Hascall VC (1983) Proteoglycans in primate arteries. III. Characterization of the proteoglycans synthesized by arterial smooth muscle cells in culture. J Cell Biol 96:167–176

    Google Scholar 

  • Yamagata M, Yamada KM, Yoneda M, Suzuki S, Kimata K (1986) Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. J Biol Chem 261:13526–13535

    Google Scholar 

  • Yamagata M, Kimata K, Oike Y, Tani K, Maeda N, Yoshida K, Shimomura Y, Yoneda M, Suzuki S (1987) A monoclonal antibody that specifically recognizes a glucuronic acid 2-sulfatecontaining determinant. J Biol Chem 262:4146–4152

    Google Scholar 

  • Yamagata M, Suzuki S, Akiyama SK, Yamada KM, Kimata K (1989) Regulation of cell-substrate adhesion by proteoglycans immobilized on extracellular substrates. J Biol Chem 264:8012–8018

    Google Scholar 

  • Zimmermann DR, Ruoslahti E (1989) Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 8:2975–2981

    Google Scholar 

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Authors and Affiliations

  1. Institute for Molecular Science of Medicine, Aichi Medical University, Nagakute, 480-11, Aichi, Japan

    Masahito Yamagata, Tamayuki Shinomura & Koji Kimata

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  1. Masahito Yamagata
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  2. Tamayuki Shinomura
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  3. Koji Kimata
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Yamagata, M., Shinomura, T. & Kimata, K. Tissue variation of two large chondroitin sulfate proteoglycans (PG-M/versican and PG-H/aggrecan) in chick embryos. Anat Embryol 187, 433–444 (1993). https://doi.org/10.1007/BF00174419

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