Calcified Tissue Research

, Volume 24, Issue 1, pp 143–149 | Cite as

Ultrahistochemical analysis of glycosaminoglycan hydrolysis in the rat periodontal ligament

II. Aryl sulfatase and bone resorption
  • C. K. Dorey
  • K. L. Bick


The distribution of aryl sulfatase in the rat periodontal ligament was investigated by ultrastructural histochemistry. In the periodontal ligament aryl sulfatase was localized specifically in osteoclasts and in vicinal perivascular macrophages. Macrophages associated with bone formation did not stain. The authors interpret this specificity as a potential marker for osteoclast differentiation from macrophages — or as a further indication of the capacity of macrophages to modulate their enzymatic complement in response to the environment. To explain the absence of aryl sulfatase in areas of bone formation we suggest that different sulfate esters are mobilized from resorbing and mineralizing matrices, and that only the enzyme associated with bone resorption is histochemically detectable with the artificial substrates currently used.

Key words

Bone Periodontal ligament Bone resorption Aryl sulfatase Mineralization 


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  1. Bach, G., Eisenberg, F., Cantz, M., Neufeld, E.F.: The defect in the Hunter syndrome: Deficiency of sulfoiduronate sulfatase. Proc. Nat. Acad. Sci. USA70, 2134–2138 (1973)PubMedGoogle Scholar
  2. Baylink, D., Wergedal, J., Thompson, E.: Loss of protein polysaccharides at sites where bone mineralization is initiated. J. Histochem. Cytochem.20, 279–292 (1972)Google Scholar
  3. Buddecke, E., Drezenick, R.: Stabilitätskonstanten der Calciumkomplexe von saueren Mucopolysacchriden. Hoppe Seyler's Z. Physiol. Chem.327, 49–64 (1962)Google Scholar
  4. Buring, K.: On the origin of cells in heterotypic bone formation. Clin. Orthop.92, 293–302 (1975)Google Scholar
  5. Carr, I.: The Macrophage. A review of ultrastructure and function. New York: Academic Press 1973Google Scholar
  6. Cohn, Z.A., Benson, B.: The in vitro differentiation of mononuclear phagocytes. II. The influence of serum on granule formation, hydrolase production and pinocytosis. J. Exp. Med.121, 835–872 (1965)PubMedGoogle Scholar
  7. Dorey, C.K., Bick, K.L.: Ultrahistochemical analysis of GAG hydrolysis in the rat periodontal ligament: Evidence for macrophage involvement in bone remodelling. Calcif. Tiss. Res.24, 135–141 (1977)Google Scholar
  8. Dorey, C.K., Newkirk, C., Bick, K.L., Gibson, W.A.: Ultrastructural histochemistry in the rat periodontal ligament. J. Dent. Res.53, 88 (1974)PubMedGoogle Scholar
  9. Engfeldt, B., Hjerpe, A.: Glycosaminoglycans of dentine and predentine. Calcif. Tiss. Res.10, 152–159 (1973)Google Scholar
  10. Farooqui, A.A.: Desulphation of hexosamine sulphates by aryl sulfatase B. Experient.32, 1242–1244 (1976)Google Scholar
  11. Fluharty, A.L., Stevens, R.L., Sanders, D.L., Kihara, H.: Arylsulfatase B deficiency in Maroteaux-Lamy syndrom cultured fibroblasts. Biochem. Biophys. Res. Comm.59, 455–461 (1974)PubMedGoogle Scholar
  12. Fluharty, A.L., Stevens, R.L., Fung, D., Peak, S., Kihara, H.: UDP-N-acetyl-galactosamine-4-sulfate sulfohydrolase activity of human aryl sulfatase B and its deficiency in the Maroteaux-Lamy syndrome. Biochem. Biophys. Res. Comm.64, 955–962 (1975)PubMedGoogle Scholar
  13. Gibson, W.A., Fullmer, H.M.: Histochemistry of the periodontal ligament. IV. The glycosidases. Periodontics40, 470–475 (1969)Google Scholar
  14. Gibson, W.A., Fullmer, H.M.: Histochemistry of the periodontal ligament. V. The aryl sulfatases. J. Periodont.41, 102–104 (1970)PubMedGoogle Scholar
  15. Goldfischer, S.: The cytochemical demonstration of lysosomal aryl sulfatase activity by light and electron microscopy. J. Histochem. Cytochem.13, 520–523 (1965)PubMedGoogle Scholar
  16. Gothlin, G., Ericsson, J.L.E.: Electron microscopic studies on the uptake and storage of thorium dioxide molecules in different cell types of fracture callus. Acta path. microbiol. Scand.81A, 523–542 (1973a)Google Scholar
  17. Gothlin, G., Ericsson, J.L.E.: On the histogenesis of the cells in fracture callus. Electron microscopic autoradiographic observations in parabiotic rats and studies on labelled monocytes. Virchow's Arch. Abt. B. Zellpath.12, 318–329 (1973b)Google Scholar
  18. Gothlin, G., Arborgh, B., Ericsson J.L.E., Helminen, H.: Histochemical and biochemical studies on localization and activity of lysosomal enzymes in fracture callus. Histochemie35, 97–110 (1973)PubMedGoogle Scholar
  19. Iwata, H., Urist, M.: Protein polysaccharides of bone morphogenetic matrix. Clin. Orthop.87, 257–274 (1972)PubMedGoogle Scholar
  20. Lamberg, S.I., Stoolmiller, A.C.: Glycosaminoglycans. A biochemical and clinical review. J. Invest. Derm.63, 433–449 (1974)PubMedGoogle Scholar
  21. Luft, J.H.: Improvement in epoxy resin embedding methods. J. Biophys. Biochem. Cytol.9, 409–414 (1961)PubMedGoogle Scholar
  22. Maroteaux, P., Lêvêque, B., Marie, J., Lamy, M.: Une nouvelle dysostose avec elimination urinarie de chondroitine-sulfate B. Presse Médicale71, 1849–1852 (1963)Google Scholar
  23. Matalon, R., Arbogast, B., Justice, P., Brandt, I., Dorfman, A.: Morquio's syndrome: Deficiency of a chondroitin sulfate N-acetyl-hexosamine sulfate sulfatase. Biochem. Biophys. Res. Comm.61, 709–715 (1974a)Google Scholar
  24. Matalon, R., Arbogast, B., Dorfman, A.: Deficiency of chondroitin sulfate N-acetyl-galactosamine-4-sulfate sulfatase in Maroteaux-Lamy syndrome. Biochem. Biophys. Res. Comm.61, 1450–1457 (1974b)PubMedGoogle Scholar
  25. McKusick, V.A.: Heritable disorders of connective tissue. 4th Ed., p. 521–664. St. Louis: Mosby 1972Google Scholar
  26. Novikoff, P.M., Novikoff, A., Quintana, N., Hauw, J.J.: Golgi apparatus, GERL and lysosomes of neurons in rat dorsal root ganglia studied by thick section and thin section cytochemistry. J. Cell Biol.50, 859–886 (1971)PubMedGoogle Scholar
  27. Porter, M.T., Fluharty, A.L., Kihara, H.: Metachromatic leukodystrophy: aryl sulfatase A deficiency in skin fibroblast cultures. Proc. Nat. Acad. Sci. (USA)62, 887–891 (1969)Google Scholar
  28. Schwartz, E.R., Ogle, R.C., Thompson, R.C.: Aryl sulfatase activities in normal and pathologic human articular cartilage. Arthritis and Rheumat.17, 455–468 (1974)Google Scholar
  29. Stumpf, D.A., Austin, J.H., Crocker, A.C., LaFrance, M.: Mucopolysaccharidoses type IV (Maroteaux-Lamy Syndrome). Sulfatase B deficiency in tissues. Am. J. Dis. Child.126, 747–755 (1973)PubMedGoogle Scholar
  30. Thyberg, J., Nilsson, S., Freiberg, U.: Electron microscopic and enzyme cytochemical studies on the guinea pig metaphysis with special reference to the lysosomal system of different cell types. Cell Tiss. Res.156, 273–299 (1975)Google Scholar
  31. Tudball, N., Davidson, E.A.: Isolation of a novel sulfatase from rat liver. Biochim. Biophys. Acta171, 113–120 (1968)Google Scholar
  32. Vaes, G., Jacques, P.: Studies on bone enzymes. The assay of acid hydrolases and other enzymes in bone tissue. Biochem. J.97, 380–402 (1965)Google Scholar
  33. van Furth, R., Chon, A.Z., Hirsch, J.G. Humphrey, J.H., Spector, W.G., Langevoort, H.L.: The mononuclear phagocyte system: a new classification of macrophages, monocytes and their precursor cells. Bull. Wld. Helth. Org.46, 845–852 (1972)Google Scholar
  34. Vejlens, L.: Glycosaminoglycans of human bone tissue. I. Pattern of compact bone in relation to age. Calcif Tiss. Res.7, 175–190 (1971)Google Scholar
  35. Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol.25, 407–408 (1965)PubMedGoogle Scholar
  36. Wachsmuth, E.D.: Aminopeptidase as a marker for macrophage differentiation. Exp. Cell Res.96, 409–412 (1975)PubMedGoogle Scholar
  37. Walker, D.G.: Bone resorption restored in osteopetrotic mice by transplants of normal bone marrow and spleen cells. Science190, 784–785 (1975a)PubMedGoogle Scholar
  38. Walker, D.G.: Spleen cells transmit osteopetrosis in mice. Science190, 785–787 (1975b)PubMedGoogle Scholar
  39. Yoshiki, S., Umeda, T., Kurahshi, Y.: An effective reactivation of alkaline phosphatase in hard tissue completely decalcified for light and electron microscopy. Histochemie29, 296–304 (1972)PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1977

Authors and Affiliations

  • C. K. Dorey
    • 1
    • 2
  • K. L. Bick
    • 1
    • 2
  1. 1.Department of BiologyGeorgetown UniversityWashington, D.C.USA
  2. 2.Department of PathologyLitton Bionetics, Inc.KensingtonUSA

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