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An investigation of ageing in human costal cartilage

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Summary

Changes in human costal cartilage with increasing age (2–81 years) have been studied in the optical and electron microscope using routine and histochemical techniques.

Concurrent with increasing age, chondrocytes undergo degeneration which is characterized initially by the accumulation of lipidic material within cells and, subsequently, by the formation of a halo around degenerating chondrocytes. The halo material is composed of electron dense bodies, amorphous material, and collagen fibrils. Both electron dense bodies and the amorphous material are of cellular origin and they have similar histochemical responses.

Using histochemical techniques in the optical and in the electron microscope, it has been shown that chondroitin sulfate decreases with increasing age, while a hyaluronidase resistant material (presumably keratan sulfate) increases, initially in the central zone, and subsequently in the peripheral zones. Hyaluronidase resistant material is minute or absent in the central zone of aged cartilage.

The genesis of collagen fibrils progresses from thin unbanded collagen-like fibrils in the pericellular lacunae of chondrocytes in young specimens to thick fibrils (sometimes in excess of 0.5 μ) with a period of 640 Å in ageing cartilage. Aggregation of collagen fibrils seems to be related at least initially to the preponderance of matrix granules and beaded filaments which have been shown to originate intracellularly in vacuoles formed in degenerating mitochondria. Both of these structures contain glycosaminoglycans and, with increasing age, glycosaminoglycans decrease while collagen fibrils aggregate. In old age, the amorphous material, and possibly the content of disrupting electron dense bodies, seem to give origin to some collagen fibrils. This and other mechanisms of formation of collagen fibrils have been observed and they are discussed.

Calcification of the matrix increases with increasing age and this agrees with previous findings.

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References

  • Amprino, R., Bairati, A.: Studi sulle trasformazioni delle eartilagini 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 (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. II. North-Holland, Elsevier, Excerpta Medica 1973

  • Aureli, G., Rizzotti, M., Balderini, 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., Palfry, A. J.: Age changes in articular cartilage of rabbits. Ann. rheum. Dis. 22, 389–400 (1963)

    Google Scholar 

  • Beneke, G., Enders, 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 on 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.: The 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., Cuicchio, M., Dearden, L. C.: Investigations of ageing in costal and tracheal cartilage of rats. Z. Zellforsch. 147, 505–527 (1974b)

    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 (1974a)

  • 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 

  • Caro, L. G., Palade, G. E.: Protein synthesis, storage and discharge in the pancreatic exocrine cell. An autoradiographic study. J. Cell Biol. 20, 473–495 (1964)

    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 the colloidal iron method. J. Anat. (Lond.) 99, 427–434 (1965)

    Google Scholar 

  • Dearden, L.C.: Enhanced mineralization of the tibial epiphyseal plate in the rat following propylthiouracil treatment: A histochemical, light, and electron microscopic study. Anat. Rec. 178, 671–690 (1974)

    Google Scholar 

  • Dearden, L. C., Espinosa, T.: Comparison of mineralization of the tibial epiphyseal plate following treatment with cortisone, propylthiouracil, or after fasting: A histochemical, light, and electron microscopic study. Calcif. Tiss. Res. 15, 93–110 (1974)

    Google Scholar 

  • Dearden, L. C., Mosier, H. D., Jr.: Long-term recovery of chondrocytes in the tibial epiphyseal plate in rats after cortisone treatment. Clin. Orthop. 87, 322–331 (1972)

    Google Scholar 

  • Dearden, L. C., Mosier, H. D. Jr.: Growth retardation of the rat tibia and recovery following propylthiouracil treatment: A histochemical, light and electron microscopic study. Growth, in press (1974)

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

    Google Scholar 

  • Godman, G. C., Lane, N.: On the site of sulfation in the chondrocyte. J. Cell Biol. 21, 353–366 (1964)

    Google Scholar 

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

    Google Scholar 

  • Hay, E. D., Dodson, J. W.: Secretion of collagen by corneal epithelium I. Morphology of the collagenous products produced by isolated epithelia grown on frozen-killed lens. J. Cell Biol. 57, 190–213 (1973)

    Google Scholar 

  • Hough, A. J., Mottram, F. C., Sokoloff, L.: The collagenous nature of amianthoid degeneration of human costal cartilage. Amer. J. Path. 73, 201–216 (1973)

    Google Scholar 

  • Jamieson, J. D., Palade, G. E.: Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of peripheral elements of the Golgi complex. J. Cell Biol. 34, 577–596 (1967)

    Google Scholar 

  • Joel, W., Masters, Y. F., Shetlar, M. D.: 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 

  • 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 sulfate proteoglycans. 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 and New York: Academic Press 1970

    Google Scholar 

  • Marinozzi, V.: Silver impregnation of ultrathin sections for electron microscopy. J. Biophys. biochem. Cytol. 9, 121–132 (1961)

    Google Scholar 

  • Marinozzi, V.: Réaction de l'acide phosphotungstique avec la mucin et les glycoprotéines des plasma membranes. J. Microscopie 6, 68a (1967)

  • Marinozzi, V.: Phosphotungstic acid (PTA) as a stain for polysaccharides and glycoproteins in electron microscopy, p. 55. In: Electron microscopy (Bocciarelli, D. S., ed.), vol. II. Rome: Tipografia Poliglotta Vaticana 1968

    Google Scholar 

  • 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 aging 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, R.: 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 

  • Mihatsch, M. J., Riede, U. N., Bianchi, L.: Ultrastrukturelle Veränderung des Knorpels im Falle der Phenacetin-Pseudo-Ochronose und der Alkaptonurie. Virchows Arch. Abt. B 14, 307–312 (1973)

    Google Scholar 

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

    Google Scholar 

  • Neutra, M., Leblond, C. P.: Radiographic comparison of the uptake of galactose 3H and glucose 3H in the Golgi region of various cells secreting glycoproteins or mucopolysaccharides. J. Cell Biol. 30, 137–150 (1966)

    Google Scholar 

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

    Google Scholar 

  • Quintarelli, G.: The chemical physiology of mucopolysaccharides. First edition London: J. & A. Churchill Ltd. 1968

    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 

  • Rambourg, A., Hernandez, W., Leblond, C. P.: Detection of complex carbohydrates in the Golgi apparatus of rat cells. J. Cell Biol. 40, 395–414 (1969)

    Google Scholar 

  • Revel, J. P., Hay, E. D.: An autoradiographic and electron microscopic study of collagen synthesis in differentiating cartilage. Z. Zellforsch. 61, 110–144 (1963)

    Google Scholar 

  • Rohr, H., Walter, S.: Die Mucopolysaccharidsynthese in ihrer Beziehung zur submikroskopischen Struktur der Knorpelzelle. Acta anat. (Basel) 64, 223–234 (1966)

    Google Scholar 

  • Schaffer, J.: Die Stützgewebe. In: Handbuch der mikroskopischen Anatomie des Menschen (W. v. Möllendorff, Hsrg.), 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, 221–223 (1965)

    CAS  PubMed  Google Scholar 

  • Scott, J. E., Dorling, J., Quintarelli, G.: Differential staining of acid glycosaminoglycans by Alcian blue in salt solutions. Biochem. J. 90, 4–5 (1964)

    Google Scholar 

  • Sheldon, H., Kimball, F. B.: Studies on cartilage III. The occurrence of collagen within vacuoles of the Golgi apparatus. J. Cell Biol. 12, 599–613 (1962)

    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., Silberberg, M., Vogel, A., Wettstein, W.: Ultrastructure of articular cartilage of mice of various ages. Amer. J. Anat. 109, 251–275 (1961)

    Google Scholar 

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

    Google Scholar 

  • Sisca, R. F., Provenza, D. V.: Initial dentin formation in human deciduous teeth. An electron microscopic 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.), Centre National de la Recherche Scientifique, Paris. 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 from dentine. 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. C., 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.: Ultrastructural localization of aryl sulfatase activity in the epiphyseal plate. J. Ultrastruct. Res. 38, 332–342 (1972)

    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 

  • Thyberg, J., Friberg, U.: Electron microscopic enzyme histochemical studies on the cellular genesis of matrix vesicles in the epiphyseal plate. J. Ultrastruct. Res. 41, 43–59 (1972)

    Google Scholar 

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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 and extensive technical assistance. — To Dr. A. Ascenzi, Director 1° Istituto di Anatomia e Istologia Patologica, and to Dr. C. Cavallero, Director, 2° Istituto di Anatomia e Istologia Patologica, Università di Roma, the senior author would like to express his appreciation for the use of equipment and facilities pursuant to this investigation, while on sabbatical leave from the University of California, Irvine, College of Medicine. — We wish to extend our thanks to the Italian National Research Council for supporting this study.

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

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Dearden, L.C., Bonucci, E. & Cuicchio, M. An investigation of ageing in human costal cartilage. Cell Tissue Res. 152, 305–337 (1974). https://doi.org/10.1007/BF00223953

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