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Vectorial sequence of mineralization in the turkey leg tendon determined by electron microscopic imaging

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Summary

Turkey leg tendons were used as a model tissue to study the spatial and temporal relationships of mineral deposition between matrix vesicles and collagen fibrils by various electron microscopic techniques—bright field, selected-area dark field (SADF), and electron spectroscopic imaging (ESI). These latter imaging techniques enabled the direct localization and spatial distributions of both apatite crystals and atomic elements (Ca, P) within matrix vesicles and collagen. In longitudinal planes of section, a consistent vectorial gradient of mineralization was observed which started with the first localization of apatite mineral in matrix vesicles; with further development, the mineral spread from the vesicle to the extravesicular interstices and then into the adjacent collagen fibrils. Once intrafibrillar, the mineral was observed to advance both laterally and axially. The association of vesicle/collagen mineral was examined by ESI analysis of Ca and P elemental maps and appeared as a continuum between the vesicles and the adjacent collagen fibrils. Similarly, an intimate spatial relationship was observed between the mineral of vesicles and collagen in transversely cut sections of tendon. The sequential development of this mineralized matrix is discussed in light of matrix vesicle/collagen interactions.

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References

  1. Glimcher MJ (1959) Molecular biology of mineralized tissues with particular reference to bone. Rev Mod Phys 31:359–393

    Article  CAS  Google Scholar 

  2. Glimcher MJ (1984) Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Phil Trans R Soc Lond B 304:479–508

    CAS  Google Scholar 

  3. Glimcher MJ (1985) The role of collagen and phosphoproteins in the calcification of bone and other collagenous tissues. In: Rubin RP, Weiss G, Putney JW, Jr. (eds) Calcium in Biological Systems. Plenum, New York, pp 607–616

    Google Scholar 

  4. Anderson HC (1969) Vesicles associated with calcification in the matrix of epiphyseal cartilage. J Cell Biol 41:59–72

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  6. Hunziker EB, Herrmann W, Cruz-Orive LM, Arsenault AL (1989) Image analysis of electron micrographs relating to mineralization in calcifying cartilage: Theoretical considerations. J Elect Microsc Tech 11:9–15

    Article  CAS  Google Scholar 

  7. Bernard GW (1970) Initial calcification of cementum. IADR (abstract #517)

  8. Arsenault AL, Robinson BW (1989) The dentino-enamel junction: a structural and microanalytical study of early mineralization. Calcif Tissue Int 45:111–121

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  10. Arsenault AL, Ottensmeyer FP, Heath IB (1988) An electron microscopic and spectroscopic study of murine epiphyseal cartilage: analysis of fine structure and matrix vesicles preserved by slam freezing and freeze substitution. J Ultrastruct Mol Struct Res 98:32–47

    Article  PubMed  CAS  Google Scholar 

  11. Arsenault AL, Hunziker EB (1988) Electron microscopic analysis of mineral deposits in the calcifying epiphyseal growth plate. Calcif Tissue Int 42:119–126

    PubMed  CAS  Google Scholar 

  12. Arsenault AL (1988) Crystal-collagen relationships in calcified turkey leg tendons visualized by selected-area dark field electron microscopy. Calcif Tissue Int 43:202–212

    Article  PubMed  CAS  Google Scholar 

  13. Landis WJ (1986) A study of calcification in the leg tendons from the domestic turkey. J Ultrastruct Mol Struct Res 94:217–238

    Article  PubMed  CAS  Google Scholar 

  14. Landis WJ (1985) Temporal sequence of mineralization in calcifying turkey leg tendon. In: Butler WT (ed) The chemistry and biology of mineralized tissues. Ebsco Media, Inc. Birmingham, Alabama, pp 360–363

    Google Scholar 

  15. Hodge AJ, Schmitt FO (1960) The charge profile of the tropocollagen macromolecule and the packing arrangement in native-type collagen fibrils. Proc Natl Acad Sci 46:186–197

    Article  PubMed  CAS  Google Scholar 

  16. Bonucci E (1971) The locus of initial calcification in cartilage and bone. Clin Orthop Rel Res 78:108–139

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  18. Ali SY, Wisby A, Craig Grey J (1978) Electron probe analysis of cryosections of epiphyseal cartilage. Metab Bone Dis Rel Res 1:97–103

    Article  Google Scholar 

  19. Johnson LC (1960) Mineralization of turkey leg tendon. I. Histology and histochemistry of mineralization. In: Sognnaes RF (ed) Calcification in biological systems. Amer Assn Adv Sci, Washington, DC, pp 117–128

    Google Scholar 

  20. Nylen MU, Scott DB, Mosley VM (1960) Mineralization of the turkey leg tendon. II. Collagen-mineral relationships revealed by electron and x-ray microscopy. In: Sognnaes RF (ed) Calcification in biological systems. Amer Assn Adv Sci, Washington, DC, pp 129–142

    Google Scholar 

  21. Landis WJ, Arsenault AL (in press) Vesicle- and collagen-mediated calcification in the turkey leg tendon. In: Glimcher MJ (ed) The chemistry and biology of mineralized tissues, Chatham, Massachusetts

  22. Arsenault AL, Ottensmeyer FP (1983) Quantitative spatial distributions of calcium, phosphorus, and sulfur in calcifying epiphysis by high resolution electron spectroscopic imaging. Proc Natl Acad Sci USA 80:1322–1326

    Article  PubMed  CAS  Google Scholar 

  23. Arsenault AL (1985) Fine structure and elemental maps of the calcifying epiphysis preserved by slam freezing and freeze substitution. In: Butler WT (ed) The chemistry and biology of mineralized tissues. Ebsco Media, Inc, Birmingham Alabama, pp 364–367

    Google Scholar 

  24. Arsenault AL, Hunziker EB (1986) Electron microscopic and spectroscopic analysis of matrix vesicles from the epiphyseal growth plate: cryogenic tissue preparation. In: Ali SY (ed) Cell-mediated calcification and matrix vesicles. Experta Medica, Netherlands, pp 17–20

    Google Scholar 

  25. Akisaka T, Kawaguichi H, Subita GP, Shigenaga Y, Gay CV (1988) Ultrastructure of matrix vesicles in chick growth plate as revealed by quick freezing and freeze substitution. Calcif Tissue Int 42:383–393

    PubMed  CAS  Google Scholar 

  26. Landis WJ, Glimcher MJ (1982) Electron optical and analytical observations of rat growth plate cartilage prepared by ultracryomicrotomy: the failure to detect a mineral phase in matrix vesicles and the identification of heterodispersed particles as the initial solid phase of calcium phosphate deposited in the extracellular matrix. J Ultrastruct Res 78:227–268

    Article  PubMed  CAS  Google Scholar 

  27. Wuthier RE (1982) A review of the primary mechanism of endochondral calcification with special emphasis on the role of cells, mitochondria and matrix vesicles. Clin Orthop Rel Res 169:219–242

    CAS  Google Scholar 

  28. Wuthier RE (1988) Mechanism of matrix vesicle-mediated mineralization of cartilage. ISI Atlas of Science, Biochem 1:231–241

    CAS  Google Scholar 

  29. Hinek A, Reiner A, Poole RA (1987) The calcification of cartilage matrix in chondrocyte culture: studies of the C-propeptide of type II collagen (chondrocalcin). J Cell Biol 104:1435–1441

    Article  PubMed  CAS  Google Scholar 

  30. Poole AR, Pidoux I, Reiner A, Choi H, Rosenberg LC (1984) Association of an extracellular protein (chondrocalcin) with the calcification of cartilage in endochondral bone formation. J Cell Biol 98:54–65

    Article  PubMed  CAS  Google Scholar 

  31. Glimcher MJ, Brickley-Parsons D, Kossiva D (1979) Phosphopeptides and γ-carboxyglutamic acid-containing peptides in calcified turkey tendon: their absence in uncalcified tendon. Calcif Tissue Int 27:281–284

    Article  PubMed  CAS  Google Scholar 

  32. Veis A (1985) Phosphoproteins of dentin and bone: do they have a role in matrix mineralization? in: Butler WT (ed) The chemistry and biology of mineralized tissues. Ebsco Media, Birmingham, Alabama, pp 170–176

    Google Scholar 

  33. Termine JD, Kleinman HK, Whitson WS, Conn KM, McGarvey ML, Martin GR (1981) Osteonectin, a bone specific protein linking mineral to collagen. Cell 26:99–105

    Article  PubMed  CAS  Google Scholar 

  34. Weinstock A, King PC, Wuthier RE (1967) The ion-binding characteristics of reconstituted collagen. Biochem J 102: 983–988

    PubMed  CAS  Google Scholar 

  35. Arsenault AL (1990) Image analysis of collagen-associated mineral distribution in cryogenically prepared turkey leg tendons. Calcif Tissue Int (in press)

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Authors and Affiliations

  1. Department of Anatomy, University of British Columbia, Vancouver, British Columbia, Canada

    A. Larry Arsenault

  2. Department of Medical Biophysics, Ontario Cancer Institute, Toronto, Ontario, Canada

    Brad W. Frankland & F. Peter Ottensmeyer

Authors
  1. A. Larry Arsenault
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  2. Brad W. Frankland
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  3. F. Peter Ottensmeyer
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Arsenault, A.L., Frankland, B.W. & Ottensmeyer, F.P. Vectorial sequence of mineralization in the turkey leg tendon determined by electron microscopic imaging. Calcif Tissue Int 48, 46–55 (1991). https://doi.org/10.1007/BF02555795

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  • DOI: https://doi.org/10.1007/BF02555795

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