Skip to main content
SpringerLink
Log in

Histochemical and electron microscope investigations on medullary bone

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Folliculin administration to pigeons stimulates the development of medullary bone in marrow spaces of the femora and other long bones. It is a specialized osseus tissue not devoted to mechanical functions and which is rapidly reabsorbed before egg-shell formation.

Medullary bone is formed and reabsorbed in the same way as other types of bone. Consequently, because of its very rapid rate of formation and resorption, it represents an ideal tissue for studying osteoblastic, osteoclastic and osteocytic activity, and the calcification process.

Medullary bone is deeply stained by PAS, Alcian blue and colloidal iron and is metachromatic after toluidine blue staining. This shows that its interfibrillary ground substance contains relatively high amounts of glycoproteins and acid proteoglycans.

Calcification initially occurs in matrix vesicles (or calcifying globules) which are very numerous between the collagen fibrils of the osteoid tissue, and successively spreads into the surrounding interfibrillar matrix. Here, the crystals are closely related to thin, filament-like organic structures which seem to be components of ground substance proteoglycans.

These findings confirm that in medullary bone, as in other types of calcifying tissue, the inorganic substance is initially laid down within calcifying globules and is successively closely related to organic, non-collagenous, filamentous organic structures (crystal ghosts) which probably represent a framework for calcium salt deposition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, H. C.: Electron microscopic studies of induced cartilage development and calcification. J. Cell Biol. 35, 81–101 (1967)

    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. North-Holland, Excerpta Medica, Elsevier 1973

  • Appleton, J.: Ultrastructural observations on early cartilage calcification. The use of chromium sulphate in decalcification. Calcif. Tiss. Res. 5, 270–276 (1970)

    Google Scholar 

  • Ascenzi, A., Bonucci, E.: The tensile properties of single osteons. Anat. Rec. 158, 375–386 (1967)

    Google Scholar 

  • Ascenzi, A., Bonucci, E.: The compressive properties of single osteons. Anat. Rec. 161, 377–392 (1968)

    Google Scholar 

  • Ascenzi, A., Bonucci, E.: The shearing properties of single osteons. Anat. Rec. 172, 499–510 (1972)

    Google Scholar 

  • Ascenzi, A., Bonucci, E., Steve-Bocciarelli, D.: An electron microscope study of osteon calcification. J. Ultrastruct. Res. 12, 287–303 (1965)

    Google Scholar 

  • Ascenzi, A., François, C., Steve-Bocciarelli, D.: On the bone induced by estrogens in birds. J. Ultrastruct. Res. 8, 491–505 (1963)

    Google Scholar 

  • Baud, A.: Morphologie et structure inframicroscopique des ostéocytes. Acta anat. (Basel) 51, 209–225 (1962)

    Google Scholar 

  • Baud, C. A., Dupont, D. H.: The fine structure of the osteocytes in the adult compact bone. In: Fifth Intern. Congr. Electron Microscopy. New York: Academic Press 1962

    Google Scholar 

  • Benoit, J., Clavert, J.: Etude histologique de l'ossification folliculinique chez les oiseaux. Bull. Histol. Techn. micr. 20, 25–42 (1943)

    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 intramembranous osteogenesis. Amer. J. Anat. 125, 271–290 (1969)

    Google Scholar 

  • Bloom, M. A., Domm, L. V., Nalbandov, A. V., Bloom, W.: Medullary bone of laying chickens. Amer. J. Anat. 102, 411–453 (1958)

    Google Scholar 

  • Bloom, W., Bloom, M. A., McLean, F. C.: Calcification and ossification. Medullary bone changes in the reproductive cycle of female pigeons. Anat. Rec. 87, 443–475 (1941)

    Google Scholar 

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

    Google Scholar 

  • Bonucci, E.: Further investigation on the organic/inorganic relationships in calcifying cartilage. Calcif. Tiss. Res. 3, 38–54 (1969)

    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 (1971)

    Google Scholar 

  • Bonucci, E.: The organic-inorganic relationships in calcified organic matrices. In: Physicochimie et cristallographie des apatites d'intérêt biologiques. Colloque No. 230. Paris: CNRS 1973

    Google Scholar 

  • Bonucci, E.: The organic-inorganic relationships in bone matrix undergoing osteoclastic resorption. Calcif. Tiss. Res. 16, 13–36 (1974)

    Google Scholar 

  • Bonucci, E.: Histochemical and ultrastructural investigations on calcification of the aorta. In: Extracellular matrix influences on gene expression (Slavkin, H. C. and Greulich, R. C., eds.). New York-San Francisco-London: Academic Press 1975

    Google Scholar 

  • Bonucci, E., Derenzini, M., Marinozzi, V.: The organic-inorganic relationship in calcified mitochondria. J. Cell Biol. 59, 185–211 (1973)

    Google Scholar 

  • Bonucci, E., Sadun, R.: Dihydrotachysterol-induced aortic calcification. A histochemical and ultrastructural investigation. Clin. Orthop. 107, 283–294 (1975)

    Google Scholar 

  • Cameron, D. A.: The fine structure of osteoblasts in the metaphysis of the tibia of the young rat. J. biophys. biochem. Cytol. 9, 583–595 (1961)

    Google Scholar 

  • Cameron, D. A.: The fine structure of bone and calcified cartilage. Clin. Orthop. 26, 199–228 (1963)

    Google Scholar 

  • Candlish, J. K., Holt, F. J.: The proteoglycans of fowl cortical and medullary bone. Comp. Biochem. Physiol. 40 B, 283–293 (1971)

    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., Lowell, D.: Acid mucopolysaccharides in electron microscopy. The use of the colloidal iron method. J. Anat. (Lond.) 99, 427–434 (1965)

    Google Scholar 

  • Dallemagne, M. J., Govaerts, J., Melon, J.: Influence de la folliculine sur le métabolisme calcique du pigeon, étudiée a l'aide du radiocalcium. Arch. int. Physiol. 58, 157–187 (1969)

    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 

  • Dudley, H. R., Spiro, D.: The fine structure of bone cells. J. biophys. biochem. Cytol. 11, 627–649 (1961)

    Google Scholar 

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

    Google Scholar 

  • François, C.: La composition minérale et le degré de minéralisation d'un os jeune, l'os folliculinique du pigeon. Bull. Soc. Chim. biol. (Paris) 42, 259–267 (1960)

    Google Scholar 

  • Gonzales, F., Karnovsky, M. J.: Electron microscopy of osteoclasts in healing fractures of rat bone. J. biophys. biochem. Cytol. 9, 299–316 (1961)

    Google Scholar 

  • Hancox, N. M.: Biology of bone. Cambridge: The University Press 1972

    Google Scholar 

  • Höhling, H. J., Ashton, B. A., Köster, H. D.: Quantitative electron microscopic investigations of mineral nucleation in collagen. Cell Tiss. Res. 148, 11–26 (1974)

    Google Scholar 

  • Höhling, H. J., Scholz, F., Boyde, A., Heine, H. G., Reimer, L.: Electron microscopical and laser diffraction studies on the nucleation and growth of crystals in the organic matrix of dentine. Z. Zellforsch. 117, 381–393 (1971)

    Google Scholar 

  • Jande, S. S.: Effects of parathormone on osteocytes and their surrounding bone matrix. An electron microscopic study. Z. Zellforsch. 130, 463–470 (1972)

    Google Scholar 

  • Jande, S. S., Bélanger, L. F.: Electron microscopy of osteocytes and the pericellular matrix in rat trabecular bone. Calcif. Tiss. Res. 6, 280–289 (1971)

    Google Scholar 

  • Jande, S. S., Bélanger, L. F.: The life cycle of the osteocyte. Clin. Orthop. 94, 281–305 (1973)

    Google Scholar 

  • Katchburian, E.: Membrane-bound bodies as initiators of mineralization of dentine. J. Anat. (Lond.) 116, 285–302 (1973)

    Google Scholar 

  • Kyes, P., Potter, T. S.: Physiological marrow ossification in female pigeons. Anat. Rec. 60, 377–379 (1934)

    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 

  • 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 olysaccharides and glycoproteins in electron microscopy. In: Electron microscopy (Bocciarelli, D. S., ed.), vol. II. Tipografia Poliglotta Vaticana: Rome 1968

    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 

  • Mélon, J., Govaerts, J., Dallemagne, M. J.: Influence de la folliculine sur le métabolisme calcique du pigeon, étudiée à l'aide du radiocalcium. Experientia (Basel) 5, 331–333 (1949)

    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 reaction. Lab. Invest. 7, 566–576 (1958)

    Google Scholar 

  • Mueller, W. J., Brubaker, R. L., Caplan, M. D.: Egg shell formation and bone resorption in laying hens. Fed. Proc. 28, 1851–1856 (1969)

    Google Scholar 

  • Pugliarello, M. C., Vittur, F., de Bernard, B., Bonucci, E., Ascenzi, A.: Chemical modifications in osteones during calcification. Calcif. Tiss. Res. 5, 108–114 (1970)

    Google Scholar 

  • Rambourg, A.: Morphological and histochemical aspects of glycoproteins at the surface of animals cells. Int. Rev. Cytol. 31, 57–114 (1971)

    Google Scholar 

  • Remagen, W., Höhling, H. J., Hall, T. T., Caesar, R.: Electron microscopical and microprobe observations on the cell sheath of stimulated osteocytes. Calcif. Tiss. Res. 4, 60–68 (1969)

    Google Scholar 

  • Scherft, J. P.: The Lamina Limitans of the organic matrix of calcified cartilage and bone. J. Ultrastruct. Res. 38, 318–331 (1972)

    Google Scholar 

  • Schulz, A., Donath, K., Delling, G.: Ultrastruktur und Entwicklung des Corticalisosteocyten. Tierexperimentelle Untersuchungen an der Rattentibia. Virchows Arch. Abt. A 364, 347–356 (1974)

    Google Scholar 

  • Scott, B. L.: The occurrence of specific cytoplasmic granules in the osteoclast. J. Ultrastruct. Res. 19. 417–431 (1967)

    Google Scholar 

  • Scott, B. L., Pease, D. C.: Electron microscopy of the epiphyseal apparatus. Anat. Rec. 126, 465–495 (1956)

    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., 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 young rabbit. J. Cell Sci. 6, 843–864 (1970)

    Google Scholar 

  • Taylor, T. G.: Calcium-endocrine relationships in the laying hen. Proc. Nutr. Soc. 24, 49–54 (1964)

    Google Scholar 

  • Taylor, T. G., Bélanger, L. F.: The mechanism of bone resorption in laying hens. Calcif. Tiss. Res. 4, 162–173 (1969)

    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 

  • Tonna, E. A.: Electron microscopic evidence of alternating osteocytic-osteoclastic and osteoplastic activity in the perilacunar walls of aging mice. Connect. Tiss. Res. 1, 221–230 (1972)

    Google Scholar 

  • Urist, M. R.: The effect of calcium deprivation upon the blood adrenal cortex, ovary and skeleton in domestic fowl. Recent Progr. Hormone Res. 15, 455–477 (1959)

    Google Scholar 

  • Urist, M. R., McLean, F. C.: The partition and binding of calcium in the serum of the laying hen and of the estrogenized rooster. Endocrinol. 63, 570–585 (1958)

    Google Scholar 

  • Wassermann, F., Yaeger, J. A.: Fine structure of the osteocyte capsule and of the wall of the lacunae in bone. Z. Zellforsch. 67, 636–652 (1965)

    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 

Download references

Author information

Authors and Affiliations

  1. 1∘ Istituto di Anatomia e Istologia Patologica, Policlinico Umberto I, Roma, Italy

    E. Bonucci & G. Gherardi

Authors
  1. E. Bonucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Gherardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The present investigation has been supported by grants from the Italian National Research Council.

The authors are indebted to Miss Giuliana Silvestrini and Mr. Lucio Virgilii for their expert technical assistance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonucci, E., Gherardi, G. Histochemical and electron microscope investigations on medullary bone. Cell Tissue Res. 163, 81–97 (1975). https://doi.org/10.1007/BF00218592

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00218592

Key words

Search

Navigation