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Immunohistochemical localization of collagenous proteins in cartilaginous tumors: characteristic distribution of type IX collagen

  • Original Papers
  • Experimental Oncology
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Abstract

The distinctive tissue localization of collagen types, particularly of type IX collagen in human cartilaginous tumors (10 cases of enchondroma and 15 cases of chondrosarcoma including 3 cases of secondary chondrosarcoma) was examined immunohistochemically using affinitypurified antibodies against types I, II, III, V, VI, and IX collagen, in comparison with that in human fetal cartilage. In fetal cartilage matrix, types II and IX collagen were diffusely distributed, while types I, III, and V collagens were not present. In the matrices of enchondromas and primary chondrosarcomas, types II and IX collagens were also diffusely distributed, but with some areas of irregular type IX collagen deposits. The secondary chondrosarcoma simulated normal fetal cartilage in the distribution pattern of types II and IX collagen, unlike the pattern in primary chondrosarcoma, where types II and IX collagen were decreased and poorly immunostained, whereas non-cartilaginous interstitial collagens (I, III, and V) appeared diffusely in the matrix, increasing with the grade of malignancy. These findings suggest that neoplastic cartilage is characterized initially by an uneven distribution of type IX collagen, prior to any alteration of other types of collagen; the diverse expressions of intercellular components in cartilaginous tumors may be one indicator for malignancy.

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Abbreviations

High-M r :

high molecular mass

low-M r :

low molecular mass

References

  • Bruckner P, Vaughan L, Winterhalter KH (1985) Type IX collagen sternal cartilage of chicken embryo contains covalently bound glycosaminoglycans. Proc Natl Acad Sci USA 82:2608–2612

    Google Scholar 

  • Bruckner P, Mendler M, Steinmann B, Huber S, Winterhalter KH (1988) The structure of human collagen type IX and its organization in fetal and infanct cartilage fibrils. J Biol Chem 263:16911–16917

    Google Scholar 

  • Buckwalter JA (1983) The structure of human chondrosarcoma proteoglycans. J Bone Joint Surg 65:958–974

    Google Scholar 

  • Burgeson RE, Morris NP (1987) The collagen family of proteins. In: Uitto J, Perejda AJ (eds) Connective tissue disease: molecular pathology of the extracellular matrix, Dekker, New York pp 3–28

    Google Scholar 

  • Cizdziel PE, Hosoi J, Montgomery JC, Wiseman RW, Barrett JC (1991) Loss of a tumor suppressor gene function is correlated with downregulation of chondrocyte-specific collagen expression in Syrian hamster embryo cells. Mol Carcinog 4:14–24

    Google Scholar 

  • Dublet B, Rest M van der (1987) Type XII collagen is expressed in embryonic chick tendons. Isolation of pepsin-derived fragments. J Biol Chem 262:17724–17727

    Google Scholar 

  • Evans HL, Ayala AG, Romsdahl MM (1977) Prognostic factors in chondrosarcoma of bone. A clinicopathologic analysis with emphasis on histologic grading. Cancer 40:818–831

    Google Scholar 

  • Gionti E, Capasso O, Cancedda R (1983) The culture of chick embryo chondrocytes and the control of their differentiated functions in vitro. J Biol Chem 258:7190–7194

    Google Scholar 

  • Gordon MK, Gerecke DR, Olsen BR (1987) Type XII collagen: distinct extracellular matrix component discovered by cDNA cloning. Proc Natl Acad Sci USA 84:6040–6044

    Google Scholar 

  • Hata R, Ninomiya Y, Nagai Y, Tsukada Y (1980) Biosynthesis of interstitial types of collagen by albumin-producing rat liver parenchymal cell (hepatocyte) clones in culture. Biochemistry 19:169–176

    Google Scholar 

  • Herwig J, Roessner A, Buddecke E (1986) Isolation and characterization of proteoglycans and glycosaminoglycans from human chondrosarcoma. Exp Mol Pathol 45:118–127

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) A comparative study of the peroxidase-antiperoxidase method and an avidin-biotin-complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clin Pathol 75:734–738

    Google Scholar 

  • Kreicbergs A, Boquist L, Borssén B, Larsson S-E (1982) Prognostic factors in chondrosarcoma. A comparative study of cellular DNA content and clinicopathologic features. Cancer 50:577–583

    Google Scholar 

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

    Google Scholar 

  • Mayne R, Vail MS, Mayne PM, Miller EJ (1976) Changes in type of collagen synthesized as clones of chick chondrocytes grow and eventually lose division capacity. Proc Natl Acad Sci USA 73:1674–1678

    Google Scholar 

  • Mendler M, Eich-Bender SG, Vaughan L, Winterhalter KH, Bruckner P (1989) Cartilage contains mixed fibrils of collagen types II, IX, and XI. J Cell Biol 108:191–197

    Google Scholar 

  • Minamoto T, Ooi A, Okada Y, Mai M, Nagai Y, Nakanishi I (1988) Desmoplastic reaction of gastric carcinoma: a light-and electronmicroscopic immunohistochemical analysis using collagen typespecific antibodies. Hum Pathol 19:815–821

    Google Scholar 

  • Mirra JM, Gold R, Downs J, Eckardt JJ (1985) A new histologic approach to the differentiation of enchondroma and chondrosarcoma of the bones. A clinicopathologic analysis of 51 cases. Clin Orthop Relat Res 201:214–237

    Google Scholar 

  • Müller-Glauser W, Humbel B, Glatt M, Strauli P, Winterhalter KH, Bruckner P (1986) On the role of type IX collagen in the extracellular matrix of cartilage. Type IX collagen is localized to intersections of collagen fibrils. J Cell Biol 102:1931–1939

    Google Scholar 

  • Oda Y, Kawahara E, Minamoto T, Ueda Y, Ikeda K, Nagai Y, Nakanishi I (1988) Immunohistochemical studies on the tissue localization of collagen types I, III, IV, V and VI in schwannomas. Correlation with ultrastructural features of the extracellular matrix. Virchows Arch [B] 56:153–163

    Google Scholar 

  • Pal S, Strider W, Margolis R, Gallo G, Lee-Huang S (1978) Isolation and characterization of proteoglycans from human chondrosarcomas. J. Biol Chem 253:1279–1289

    Google Scholar 

  • Reese CA, Mayne R (1981) Minor collagens of chicken hyaline cartilage. Biochemistry 20:5443–5448

    Google Scholar 

  • Rennard SI, Berg R, Martin GR, Foidart JM, Robey PG (1980) Enzymelinked immunoassay (ELISA) for connective tissue components. Anal Biochem 104:205–214

    Google Scholar 

  • Sandberg M, Tamminen M, Hirvonen H, Vuorio E, Pihlajaniemi T (1989) Expression of mRNAs coding for the α 1 chain of type XIII collagen in human fetal tissues: comparison with expression of mRNAs for collagen types I, II, and III. J Cell Biol 109:1371–1379

    Google Scholar 

  • Svoboda M, Meuris S, Robyn C, Christophe J (1985) Rapid electrotransfer of proteins from polyacrylamide gel to nitrocellulose membrane using surface-conductive glass as anode. Anal Biochem 151:16–23

    Google Scholar 

  • Thonar EJ-MA, Sweet MBE, Immelman AR, Lyons G (1979) Structural studies on proteoglycan from human chondrosarcoma. Arch Biochem Biophys 194:179–189

    Google Scholar 

  • Ueda Y, Nakanishi I (1989) Immunohistochemical and biochemical studies on the collagenous proteins of human osteosarcomas. Virchows Arch [B] Cell Pathol 58:79–88

    Google Scholar 

  • Ueda Y, Oda Y, Tsuchiya H, Tomita K, Nakanishi I (1990) Immunohistological study on collagenous proteins of benign and malignant human cartilaginous tumours of bone. Virchows Arch [A] 417:291–297

    Google Scholar 

  • Vaughan L, Mendler M, Huber S, Bruckner P, Winterhalter KH, Irwin MI, Mayne R (1988) D-periodic distribution of collagen type IX along cartilage fibrils. J Cell Biol 106:991–997

    Google Scholar 

  • Yoshimura M, Jimenez SA, Kaji A (1981) Effects of viral transformation on synthesis and secretion of collagen and fibronectin-like molecules by embryonic chick chondrocytes in culture. J Biol Chem 256:9111–9117

    Google Scholar 

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Kawashima, A., Ueda, Y., Tsuchiya, H. et al. Immunohistochemical localization of collagenous proteins in cartilaginous tumors: characteristic distribution of type IX collagen. J Cancer Res Clin Oncol 120, 35–40 (1993). https://doi.org/10.1007/BF01200722

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  • DOI: https://doi.org/10.1007/BF01200722

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