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Investigations of ageing in costal and tracheal cartilage of rats

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Summary

Histological, histochemical, and ultrastructural investigations have been carried out on ageing costal and tracheal cartilage of rats. The following age groups of animals have been studied: 1, 7, 14, 20, 30, 45, 75 days, 6 months, and 2 years.

Ageing induces cellular changes which are represented by a reduction in the number of chondrocytes, a progressive increase in glycogen deposition, and processes of degeneration, the most frequent of which is the accumulation of lipidic material within large cytoplasmic vacuoles.

Changes in the intercellular matrix become evident after 20 days in costal cartilage and after 30 days in tracheal cartilage. Chondroitin sulphate decreases while keratan sulphate, whose presence is limited to the territorial matrix, increases. Glycoproteins increase slightly in young animals and then remain constant; they decrease in the subperichondrial areas in old animals.

Ultrastructurally, the matrix of cartilage of young animals contains thin collagen fibrils, most of which have no periodic banding. Roundish electron dense granules are associated with these fibrils. Irregular filaments associated with small electron-dense circular bodies are present around chondrocytes as well as within cytoplasmic vacuoles. With increasing age, and coincident with the reduction of chondroitin sulphate, the thickness of collagen fibrils increases, their period becomes evident, and the associated matrix granules decrease in number and size. Areas containing these fibrils undergo calcification, which frequently starts within roundish bodies of cellular origin. Collagen fibrils with a period of 640 Å but a highly variable thickness are often present in cartilage of adult and old rats. These fibrils seem to be due to an abnormal synthetic activity of chondrocytes.

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References

  • Amprino, R., Bairati, A.: Studi sulle trasformazioni delle cartilagini dell'uomo nell'accrescimento e nella senescenza. Z. Zellforsch. 20, 143–205 (1933)

    Google Scholar 

  • Anderson, H. C.: Vesicles in the matrix of epiphyseal cartilage: fine structure, distribution and association with calcification. In: Electron microscopy 1968 (D. S. Bocciarelli, ed.). Rome: Tipografia Poliglotta Vaticana 1968

    Google Scholar 

  • Anderson, H. C.: Vesicles associated with calcification in the matrix of epiphyseal cartilage. J. Cell Biol. 41, 59–72 (1969)

    Google Scholar 

  • Anderson, H. C.: Calcium-accumulating vesicles in the intercellular matrix of bone. In: Hard tissue growth, repair and remineralization. Ciba Found. Symp. 11. Amsterdam: North-Holland, Elsevier, Excerpta Medica 1973

    Google Scholar 

  • Anderson, H. C., Sajdera, S. W.: The fine structure of bovine nasal cartilage. Extraction as a technique to study proteoglycans and collagen in cartilage matrix. J. Cell Biol. 49, 650–663 (1971)

    Google Scholar 

  • Aureli, G., Rizzotti, M., Balduini, C., Castellani, A. A.: Variazioni di mucopolisaccaridi durante il processo di invecchiamento della cartilagine. Riv. Istoch. Norm. Patol. 15, 9–25 (1969)

    Google Scholar 

  • Barnett, C. H., Cochrane, W., Palfrey, A. J.: Age changes in articular cartilage of rabbits. Ann. rheum. Dis. 22, 389–400 (1963)

    Google Scholar 

  • Beneke, G., Endres, O. Becker, H., Kulka, R.: Über Wachstum und Degeneration des Trachealknorpels. Virchows Arch. path. Anat. 341, 365–380 (1966)

    Google Scholar 

  • Bernard, G. W.: Ultrastructural observations of initial calcification in dentine and enamel. J. Ultrastruct. Res. 41, 1–17 (1972)

    Google Scholar 

  • Bernard, G. W., Pease, D. C.: An electron microscopic study of initial membranous osteogenesis. Amer. J. Anat. 125, 271–290 (1969)

    Google Scholar 

  • Bonucci, E.: Fine structure of early cartilage calcification. J. Ultrastruct. Res. 20, 33–50 (1967)

    Google Scholar 

  • Bonucci, E.: Fine structure and histochemistry of “calcifying globules” in epiphyseal cartilage. Z. Zellforsch. 103, 192–217 (1970)

    Google Scholar 

  • Bonucci, E.: The locus of initial calcification in cartilage and bone. Clin. Orthop. 78, 108–139 (1971a)

    Google Scholar 

  • Bonucci, E.: Problemi attuali attinenti all'istochimica di talune matrici calcificanti normali e patologiche. Riv. Istoch. Norm. Patol. 17, 153–234 (1971b)

    Google Scholar 

  • Bonucci, E., Moretti, E., Pergola, M. S.: Comparison of the histochemical properties of tissues embedded in Araldite and in paraffin. Atti Accad. Naz. Lincei, Cl. Sci. Fis. Mat. Nat., in press (1974)

  • Campo, R. D., Phillips, S. J.: Electron microscopic visualization of proteoglycans and collagen in bovine costal cartilage. Calcif. Tiss. Res. 13, 83–92 (1973)

    Google Scholar 

  • Croissant, R. D.: Isolation of an intercellular matrix “RNA-protein complex” during odontogenesis. J. dent. Res. 50, 1065–1071 (1971)

    Google Scholar 

  • Curran, R. C., Clark, A. E., Lovell, D.: Acid mucopolysaccharides in electron microscopy. The use of colloidal iron method. J. Anat. (Lond.) 99, 427–434 (1965)

    Google Scholar 

  • Eisenmann, D. R., Glick, P. L.: Ultrastructure of initial crystal formation in dentin. J. Ultrastruct. Res. 41, 18–28 (1972)

    Google Scholar 

  • Hass, G. M.: Studies of cartilage IV. A morphologic and chemical analysis of ageing human costal cartilage. Arch. Path. 35, 275–284 (1943)

    Google Scholar 

  • Joel, W., Masters, Y. F., Shetlar, M. R.: Comparison of histochemical and biochemical methods for the polysaccharides of cartilage. J. Histochem. Cytochem. 4, 476–478 (1956)

    Google Scholar 

  • Kaplan, D., Meyer, K.: Ageing of human cartilage. Nature (Lond.) 183, 1267–1268 (1959)

    Google Scholar 

  • Khan, T. A., Overton, J.: Lanthanum staining of developing chick cartilage and reaggregating cartilage cells. J. Cell Biol. 44, 433–438 (1970)

    Google Scholar 

  • Larsson, Å., Bloom, G. D.: Studies on dentinogenesis in the rat. Fine structure of developing odontoblasts and predentin in relation to the mineralization process. Z. Anat. Entwickl.-Gesch. 139, 227–246 (1973)

    Google Scholar 

  • Loewi, G.: Changes in the ground substance of ageing cartilage. J. Path. Bact. 65, 381–388 (1953)

    Google Scholar 

  • Lowther, D. A., Natarajan, M.: The influence of glycoprotein on collagen fibril formation in the presence of chondroitin sulphate proteoglycan. Biochem. J. 127, 607–608 (1972)

    Google Scholar 

  • Lowther, D. A., Toole, B. P., Herrington, A. C.: Interaction of proteoglycans with tropocollagen. In: Chemistry and molecular biology of the intercellular matrix (E. A. Balazs, ed.), vol. II. London-New York: Academic Press 1970

    Google Scholar 

  • Luft, J. H.: The fine structure of hyaline cartilage matrix following ruthenium red fixative and staining. J. Cell Biol. 27, 61A (1965)

  • Mason, R. M.: Observations on the glycosaminoglycans of aging bronchial cartilage studied with Alcian blue. Histochem. J. 3, 421–434 (1971)

    Google Scholar 

  • Mason, R. M., Wusteman, F. S.: The glycosaminoglycans of human tracheobronchial cartilage. Biochem. J. 120, 777–785 (1970)

    Google Scholar 

  • Mathews, M. B., Glagov, S.: Acid mucopolysaccharide patterns in ageing human cartilage. J. clin. Invest. 45, 1103–1111 (1966)

    Google Scholar 

  • Matukas, V. J., Panner, B. J., Orbison, J. L.: Studies on ultrastructural identification and distribution of protein-polysaccharide in cartilage matrix. J. Cell Biol. 32, 365–377 (1967)

    Google Scholar 

  • Mayor, H. D., Hampton, J. C., Rosario, B.: A simple method for removing the resin from epoxy-embedded tissue. J. biophys. biochem. Cytol. 9, 909–910 (1961)

    Google Scholar 

  • Meachim, G.: Age changes in articular cartilage. Clin. Orthop. 64, 33–44 (1969)

    Google Scholar 

  • Mowry, R. W.: Improved procedure for the staining of acidic polysaccharides by Müller's colloidal (hydrous) ferric oxide and its combination with the Feulgen and the periodic acid-Schiff reactions. Lab. Invest. 7, 566–576 (1958)

    Google Scholar 

  • Pascher, M.: Zur Kenntnis der Altersveränderungen in den menschlichen Kehlkopfknorpeln, insbesondere der körnigen Entartung der Knorpelgrundsubstanz, der Vascularisations-, Resorptions-und Verknöcherungsbefunde. Virchows Arch. path. Anat. 246, 198–238 (1923)

    Google Scholar 

  • Quintarelli, G., Dellovo, M. C.: Age changes in the localization and distribution of glycosaminoglycans in human hyaline cartilage. Histochemie 7, 141–167 (1966)

    Google Scholar 

  • Rahlf, G.: Untersuchungen über Wachstum und Altern der menschlichen Rippenknorpel. Virchows Arch. Abt. A 356, 343–351 (1972)

    Google Scholar 

  • Ride, U. N.: Penicillamine-induced changes in growing rats. Amer. J. Path. 61, 249–254 (1970)

    Google Scholar 

  • Riede, U. N., Berli, T., Mihatsch, M.: Beeinflussung der enchondralen Ossifikation durch exogen verabreichte Orotsäure. Beitr. Path. 149, 13–22 (1973)

    Google Scholar 

  • Schaffer, J.: Die Stützgewebe. In: Handbuch der mikroskopischen Anatomie des Menschen (W. v. Möllendorff, Hrsg), Bd. II, H. 2. Berlin: Springer 1930

    Google Scholar 

  • Scott, J. E., Dorling, J.: Differential staining of acid glycosaminoglycans (mucopolysaccharides) by Alcian blue in salt solutions. Histochemie 5, 221–233 (1965)

    Google Scholar 

  • Seegmiller, R., Fraser, F. C., Sheldon, H.: A new chondrodystrophic mutant in mice. Electron microscopy of normal and abnormal chondrogenesis. J. Cell Biol. 48, 580–593 (1971)

    Google Scholar 

  • Silberberg, R., Hasler, M., Lesker, P. A.: Aging of the shoulder joint of guinea pigs. Electron microscopic and quantitative histochemical aspects. J. Geront. 28, 18–34 (1973)

    Google Scholar 

  • Silberberg, R., Stamp, W. G., Lesker, P. A., Hasler, M.: Aging changes in ultrastructure and enzymatic activity of articular cartilage of guinea pig. J. Geront. 25, 184–198 (1970)

    Google Scholar 

  • Sisca, R. F., Provenza, D. V.: Initial dentin formation in human deciduous teeth. An electron microscope study. Calcif. Tiss. Res. 9, 1–16 (1972)

    Google Scholar 

  • Slavkin, H. C.: The isolation and characterization of calcifying and non-calcifying matrix vesicles from dentine. In: Colloque International sur la Physicochimie et la Cristallographie des Apatites d'Interêt Biologique (G. Montel ed.). Paris: Centre National de la Recherche Scientifique, in press 1974

    Google Scholar 

  • Slavkin, H. C., Croissant, R., Bringas, P. Jr.: Epithelial-mesenchymal interactions during odontogenesis III. A simple method for the isolation of matrix vesicles. J. Cell Biol. 53, 841–849 (1972)

    Google Scholar 

  • Smith, J. W.: The disposition of proteinpolysaccharide in the epiphyseal plate cartilage of the young rabbit. J. Cell Sci. 6, 843–864 (1970)

    Google Scholar 

  • Stockwell, R. A., Scott, J. E.: Observations on the acid glycosaminoglycan (mucopolysaccharide) content of the matrix of ageing cartilage. Ann. rheum. Dis. 24, 341–350 (1965)

    Google Scholar 

  • Tang Kao, K.-Y., Leslie, J. G., Hitt, W. E., McGavack, T. H.: Isolation and partial characterization of protein polysaccharides from rat costal cartilage. Proc. Soc. exp. Biol. (N.Y.) 135, 781–784 (1970)

    Google Scholar 

  • Thyberg, J., Friberg, U.: Ultrastructure and acid phosphatase activity of matrix vesicles and cytoplasmic dense bodies in the epiphyseal plate. J. Ultrastruct. Res. 33, 554–573 (1970)

    Google Scholar 

  • Weisbrode, S. E., Capen, C. C., Nagode, L. A.: Fine structural and enzymatic evaluation of bone in thyroparathyroidectomized rats receiving various levels of vitamin D. Lab. Invest. 28, 29–37 (1973)

    Google Scholar 

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Authors and Affiliations

  1. Università di Roma I° Istituto di Anatomia ed Istologia Patologica Policlinico Umberto I°, Roma, Italia

    E. Bonucci, M. Cuicchio & L. C. Dearden

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  1. E. Bonucci
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  2. M. Cuicchio
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  3. L. C. Dearden
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Supported by grants from the Italian National Research Council. The authors are indebted to Miss Giuliana Silvestrini and to Mr. Lucio Virgilii for their expert technical assistance.

On sabbatical leave from the University of California, Irvine, College of Medicine.

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Bonucci, E., Cuicchio, M. & Dearden, L.C. Investigations of ageing in costal and tracheal cartilage of rats. Z.Zellforsch 147, 505–527 (1974). https://doi.org/10.1007/BF00307252

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