Summary
Types I, III and V collagens and proteoglycan were localized in the aorta by indirect immunofluorescence techniques. Type I collagen was more prominent in media and adventitia than in intima while type III collagen predominated in intima and media but appeared less significant in adventitia. Type V collagen was observed in intima and media only and was seen surrounding smooth muscle cells. Type I collagen was located between elastic fibres but type III collagen appeared to envelop the fibres, suggesting an interaction between elastic fibres and type III collagen.
Pretreatment of sections with testicular hyaluronidase caused no changes in staining for type I collagen, but adventitial areas showed increased staining for type III collagen. After digestion with chondroitinase ABC, intimal and medial areas showed increased staining for type III collagen. Therefore, type III collagen forms stronger interactions with proteoglycans and hyaluronic acid than does type I collagen and type III collagen in adventitia is largely masked by hyaluronic acid, while type III collagen in intima and media is associated with proteoglycan. Thus, type III collagen is a more significant component of adventitia than previously recognized. Proteoglycan was also partly localized along elastic fibres. It is, therefore, suggested that elastic fibres are coated with type III collagen, which itself is coated with proteoglycan.
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References
Bartholomew, J. S. &Anderson, J. C. (1983) Distribution of proteoglycans and hyaluronic acid in transverse sections of bovine thoracic aorta.Histochem. J. 15, 941–951.
Bauer, E. A., Jeffrey, J. J. &Eisen, A. Z. (1971) Preparation of three vertebrate collagenases in pure form.Biochem. biophys. Res. Commun. 44, 813–8.
Becker, U., Nowack, H., Gay, S., Timpl, R. (1976) Production and specificity of antibodies against the aminoterminal region in type III collagen.Immunology 31, 57–65.
Breton, M., Picard, J. &Berrou, E. (1981) Isolation and characterization of proteoglycans from pig arterial wall.Biochimie 63, 515–25.
Cappelletti, R., Del Rosso, M. &Chiarugi, V. P. (1979) A new electrophoretic method for the complete separation of all known animal glycosaminoglycans in a monodimensional run.Analyt. Biochem. 99, 311–15.
Duance, V. C., Restall, D. J., Beard, H., Bourne, F. J. &Bailey, A. J. (1977). The location of three collagen types in skeletal muscle.FEBS Lett. 79, 248–52.
Eisenstein, R. &Kuettner, K. (1976) The ground substance of the arterial wall. Part 2, electron microscope studies.Atherosclerosis 27, 37–46.
Epstein, E. H. (1974) [α1(III)]3 Human skin collagen. Release by pepsin digestion and preponderance in fetal life.J. biol. Chem. 249, 3225–31.
Gay, S., Balleisen, L., Remberger, K., Fietzek, P. P., Adelmann, B. C. &Kuhn, K. (1975) Immunohistochemical evidence for the presence of collagen type III in human arterial walls, arterial thrombi, and in leukocytes incubated with collagenin vitro.Klin. Wschr. 53, 899–902.
Gay, S., Walter, P. &Kuhn, K. (1976) Characterization and distribution of collagen types in arterial heterografts originating from the calf carotis.Klin. Wschr. 54, 889–94.
Gay, S., Rhodes, R. K., Gay, R. E. &Miller, A. J. (1981a) Collagen molecules comprised of α1(V) chains (B chains): an apparent localization in the exocytoskeleton.Coll. Rel. Res. 1, 53–8.
Gay, S., Martinez-Hernandez, A., Rhodes, R. K. &Miller, E. J. (1981b) The collagenous exocytoskeleton of smooth muscle cells.Coll. Rel. Res. 1, 377–84.
Herbert, W. J. (1973) Passive haemagglutination with special reference to the tanned cell technique. InHandbook of Experimental Immunology (edited byWeir, D. M.) pp. 20.1–20.20. Oxford: Blackwell Scientific Publications.
Johnson, G. D. &Holborrow, E. J. (1973) Immunofluorescence. InHandbook of Experimental Immunology (edited byWeir, D. M.) pp. 18.1–18.20., Oxford: Blackwell Scientific Publications.
Kapoor, R., Phelps, C. F., Cöster, L. &Fransson, L. A. (1981) Bovine aortic chondroitin sulphate-and dermatan sulphate-containing proteoglycans.Biochem. J. 197, 259–68.
Madri, J. A., Dreyer, B., Pitlick, F. A. &Furthmayr, H. (1980) The collagenous components of the subendothelium.Lab. Invest. 43, 303–15.
Mangkornkanok-mark, M., Eisenstein, R. &Bahu, R. M. (1981) Immunologic studies of bovine aortic and cartilage proteoglycans.J. Histochem. Cytochem. 29, 547–52.
McCullagh, K. G., Duance, V. C. &Bishop, K. A. (1980) The distribution of collagen types I, III and V (AB) in normal and atherosclerotic human aorta.J. Path. 130, 45–55.
McMurtrey, J., Radhakrishnamurthy, B., Dalferes, E. R., Berenson, G. S. &Gregory, J. D. (1979) Isolation of proteoglycan-hyaluronate complexes from bovine aorta.J. biol. Chem. 254, 1621–6.
Myers, D. B., Highton T. C. &Rayns, T. C. &Rayns, D. G. (1973) Ruthenium Red-positive filaments interconnecting collagen fibrils.J. Ultrastruct. Res. 42, 87–92.
Neville, D. M. (1971) Molecular weight determination of protein-dodecyl sulfate complexes by gel electrophoresis in a discontinuous buffer system.J. biol. Chem. 246, 6328–34.
Oegema, T. R., Hascall, V. C. &Eisenstein, R. (1979) Characterization of bovine aorta proteoglycan extracted with guanidine hydrochloride in the presence of protease inhibitor.J. biol. Chem. 254, 1312–8.
Poole, A. R., Pidoux, I., Reiner, A. &Rosenberg, L. (1982) An immunoelectron microscope study of the organization of proteoglycan monomer, link protein and collagen in the matrix of articular cartilage.J. Cell. Biol. 93, 921–37.
Pope, F. M., Martin, G. R., Lichtenstein, J. R., Penttinen, R. P., Gerson, B., Rowe, D. W. &McKusick, V. A., (1975) Patients with Ehlers-Danlos syndrome type IV lack type III collagen.Proc. natn. Acad. Sci. U.S.A. 72, 1314–6.
Salisbury, B. G. J. &Wagner, W. D. (1981) Isolation and preliminary characterization of proteoglycan dissociatively extracted from human aorta.J. biol. Chem. 256, 8050–7.
Schmidt, A., Prager, M., Selmke, P. &Buddecke, E. (1982) Isolation and properties of proteoglycans from bovine aorta.Eur. J. Biochem. 125, 95–101.
Scott, J. E. &Orford, C. R. (1981) Dermatan sulphate-rich proteoglycan associates with rat tail tendon collagen at the d-band in the gap region.Biochem. J. 197, 213–6.
Serafini-Fracassini, A., Wells, P. J. &Smith, J. W. (1970) Studies, on the interaction between glycosaminoglycans and fibrillar collagen. InChemistry and Molecular Biology of the Intercellular Matrix (edited byBalazs, E. A.) Vol. 2, pp. 1201–15. London, New York: Academic Press.
Smith, J. W. (1970) The disposition of protein-polysaccharide in the epiphyseal plate cartilage of the young rabbit.J. Cell Sci. 6, 843–64.
Smith, J. W. &Frame, J. (1969) Observations on the collagen and protein-polysaccharide complex of rabbit corneal stroma.J. Cell Sci. 4, 421–36.
Wight, T. N. &Ross, R. (1975) Proteoglycans in primate arteries. I. Ultrastructural localization and distribution in the intima.J. Cell Biol. 67, 660–74.
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Bartholomew, J.S., Anderson, J.C. Investigation of relationships between collagens, elastin and proteoglycans in bovine thoracic aorta by immunofluorescence techniques. Histochem J 15, 1177–1190 (1983). https://doi.org/10.1007/BF01002738
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DOI: https://doi.org/10.1007/BF01002738