Summary
It has been previously shown that the distances between the nuclei within the collagen bundles of mineralizing tissues were in good agreement with the repeat distances of the cross-banding pattern of collagen, which supports the assumption that the distances between the mineral deposits reflect to a good approximation the distances between nucleation centres on the collagen macromolecule. However, the lateral separation of the nuclei were significantly higher than the distances between close-packed triple helices.
Recently a new model of collagen aggregation has been proposed in which the smallest morphological units are subfibrils (Ø approx. 39 Å) packed in tetragonal array. This led us to measure once again the lateral separation between a) close-packed calcium phosphate needles lying in bundles at (1) the mineralizing front of mantle dentine and (2) at the mineralizing front of rat tail bone, and b) between the uranyl-lead nuclei produced in the staining of rat tail tendon.
The mean lateral distances separating these nuclei fell within the range of 39–47 Å, which is a little higher than the distances of 39 Å which separate the microholes between the subfibrils in the tetragonal packing model, which are regarded as the likely sites of nucleation. If, however, it is assumed that the forces generated during mineralization can cause the collagen fibres to swell, then the lateral separation of the nuclei and the distances between the microholes would correspond very closely.
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References
Anderson, H. C.: Electron microscopic studies of induced cartilage development and calcification. J. Cell Biol. 35, 81–101 (1967)
Appleton, J.: Ultrastructural observations on early cartilage calcification. The use of chromium sulphate in decalcification. Calcif. Tiss. Res. 5, 270–276 (1970)
Bernard, G. W.: The ultrastructural interface of bone crystals and organic matrix in woven and lamellar endochondral bone. J. dent. Res. 48, Suppl. No 5 (1968)
Bernard, G. W.: Ultrastructural observations of initial calcification in dentine and enamel. J. Ultrastruct. Res. 41, 1–17 (1972)
Bernard, G. W., Pease, D. C.: An electron microscopic study of initial intramembranous osteogenesis. Amer. J. Anat. 125, 271–290 (1959)
Bocciarelli, D. St.: Morphology of crystallites in bone. Calcif. Tiss. Res. 5, 261–269 (1970)
Bonucci, E.: Fine structure of early cartilage calcification. J. Ultrastruct. Res. 20, 33–50 (1967))
Bonucci, E.: Further investigation on the organic/inorganic relationship in calcifying cartilage. Calcif. Tiss. Res. 3, 38–54 (1969)
Bonucci, E.: The locus of initial calcification in cartilage and bone. Clin. Orthop. Nr 78, 108–139(1971)
Bouteille, M., Pease, D. C.: The tridimensional structure of native collagenous fibrils, their proteinaceous filaments. J. Ultrastruct. Res. 35, 314–338 (1971)
Eisenmann, D. R., Glick, P. L.: Ultrastructure of initial crystal formation in dentine. J. Ultrastruct. Res. 41, 18–28 (1972)
Glimcher, M. J., Travis, D.: A basic architectural principle in the organization of mineralized tissues, p. 3–37. In: Les tissues calcifiés, ed. Milhaud et al. Paris: Société d'Edition d'Enseignement Superiéur 1968
Grant, R. A., Horne, R. W., Cox, R. W.: New model for the tropocollagen macromolecule and its mode of aggregation. Nature (Lond.) 207, 882–824 (1965)
Hodge, A. J., Petruska, J. A.: Recent studies with the electronmicroscope on ordered aggregates of the tropocollagen macromolecule. In: Aspects of protein structure. Proceedings of a Symposium in Madras, 14–18th January, 1963 (G. N. Ramachandran, ed.), p. 289–300
Höhling, H. J.: Die Bauelemente von Zahnschmelz und Dentin aus morphologischer, chemischer, und struktureller Sicht. Habil.-Schrift an der Medizinischen Fakultät der Universität Münster, 1964, München: Hanser, 1966
Höhling, H. J.: Collagen mineralization in bone, dentine cementum and cartilage. Naturwissenschaften 56, 466 (1969)
Höhling, H. J., Kreilos, R., Neubauer, G., Boyde, A.: Electron microscopy and electron microscopical measurements of collagen mineralization in hard tissues. Z. Zellforsch. 122, 36–52 (1971b)
Höhling, H. J., Neubauer, G., Scholz, F., Boyde, A., Heine, H. G., Reimer, L.: Electron microscopical and laser diffraction studies of the nucleation and growth of crystals in the organic matrix of dentine. Z. Zellforsch. 117, 381–393 (1971a)
Höhling, H. J., Schöpfer, H.: Morphological investigations of apatitic nucleation in hard tissues and salivary stone. Naturwissenschaften 55, 545 (1968)
Höhling, H. J., Schöpfer, H., Neubauer, G.: Elektronenmikroskopie und Laserbeugungs-Untersuchungen zur Charakterisierung der organischen Matrix im Speichelstein und Hartgewebe. Z. Zellforsch. 108, 415–430 (1970)
Höhling, H. J., Steffens, H., Heuck, F.: Untersuchungen zur Mineralisierungsdichte im Hartgewebe mit Protein-Polysaccharid bzw. Kollagen als Hauptbestandteil der Matrix. Z. Zellforsch. 134, 283–296 (1972)
Höhling, H. J., Themann, H., Vahl, J.: Collagen and apatite in hard tissues and pathological formations from a crystal chemical point of view. Third European Symp. on Calcified Tissues, Davos 11–16th April (1965), printed in: Calcified tissues Proceedings of the Third European Symposium on Calcified Tissues p. 146–151. Berlin-Heidelberg-New York: Springer 1966.
Hulmes, D.J.S., Miller, A., Parry, D. A. D., Piez, K. A., Woodhead-Galloway, J.: Analysis of the primary structure of collagen for the origins of molecular packing. J. molec. Biol. 79, 137–148 (1973)
Koestner, W., Höhling, H. J.: Morphologische Vermessungen von Calcium-phosphat-Partikeln im sich bildenden Schmelz und Dentin im Elektronenmikroskop, bei bestmöglicher Eichung. Medical Thesis under supervision of H. J. Höhling, Inst. Med. Physics, University Münster, 1972
Luben, R. A., Sherman, J. K., Wadkins, C. L.: Studies of the mechanism of biological calcification. IV Ultrastructural analysis of calcifying tendon matrix. Calcif. Tiss. Res. 11, 39–55 (1973)
Miller, A., Parry, D.A.D.: The structure and packing of microfibrils in collagen. J. molec. Biol. 75, 441–447 (1973)
Miller, A., Wray, J. S.: Molecular packing in collagen. Nature (Lond.) 230, 437–439 (1971)
Ramachandran, G. N.: The triple helical structure of collagen. In: Aspects of protein structure, p. 39–55 (ed. G. N. Ramachandran), London-New York: Academic Press 1963
Ramachandran, G. N., Kartha, G.: Structure of collagen. Nature (Lond.) 174, 269–279 (1954)
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208 (1963)
Rich, A., Crick, F.H.C.: The molecular structure of collagen. J. molec. Biol. 3, 483–506 (1961)
Scherft, J. P.: The ultrastructure of the organic matrix of calcified cartilage and bone in embryonic mouse radii. J. Ultrastruct. Res. 23, 333–343 (1968)
Sisca, R. F., Provenza, D. V., Initial dentine formation in human deciduous teeth. Calcif. Tiss. Res. 9, 1–16 (1972)
Smith, W. J.: Molecular pattern in native collagen. Nature (Lond.) 219, 157–158 (1968)
Smith, W. J.: The disposition of proteinpolysaccharide in the epiphyseal plate cartilage of the young rabbit. J. Cell Sci. 6, 843–864 (1970)
Spanke, J., Höhling, H. J.: Morphologische Untersuchungen und Vermessungen an den Calciumphosphat-Keimen im sich bildenden Schmelz. Medical Thesis under supervision of H. J. Höhling, Inst. Med. Phys., University Münster, 1971
Sundström, B., Takuma, S.: A further contribution on the ultrastructure of calcifying cartilage. J. Ultrastruct. Res. 36, 419–424 (1971)
Takuma, S.: Ultrastructure of dentinogenesis. In: Structural and chemical organization of teeth, vol.I, p. 325–370 ed. (A.E.W. Miles). New York-London: Academic Press, 1967
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)
Tromans, W. J., Horne, R. W., Gresham, G. A., Baily, A. J.: Electron microscope studies on the structure of collagen fibres by “negative staining”. Z. Zellforsch. 58, 798–802 (1963)
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We thank the Deutsche Forschungsgemeinschaft for financial support. We thank Prof. Dr. K. Heckmann and Dr. U. Mays, Dept. of Zoology, Münster, for allowing us to use their Siemens-Elmiskop 101 sponsored by Stiftung Volkswagenwerk, and Frau Dr. Weichan, Applikationslabor Siemens, Berlin, for performing the tilting experiments at their Siemens-Elmiskop 102. We thank Fräulein Ute Sporman for valuable technical help.
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Höhling, H.J., Ashton, B.A. & Köster, H.D. Quantitative electron microscopic investigations of mineral nucleation in collagen. Cell Tissue Res. 148, 11–26 (1974). https://doi.org/10.1007/BF00224315
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DOI: https://doi.org/10.1007/BF00224315