Skip to main content

Advertisement

Log in

A correlation between the distribution of biological apatite and amino acid sequence of type I collagen

  • Laboratory Investigations
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Summary

We have determined the localization of apatite within type I collagen fibrils of calcifying turkey leg tendons by both bright field and selectedarea dark field (SADF) electron microscopy and have compared this to computer-modeled, chick type I collagen amino acid sequence data. Apatite crystals occur in both the gap and overlap zones at early stages of mineralization in an asymmetric pattern that corresponds to the polarity, N-to C-orientation, of the collagen molecule. Based on comparisons with computer-generated models of known amino acid sequence of collagen, it was determined for early stages of mineral deposition that apatite is restricted by areas of high hydrophobicity. The gap zone is less hydrophobic than the overlap zone on average but each of these zones had areas of high hydrophobicity that correlated with sites of low localization of mineral. Possible interactions between hydrophobic regions and the process of mineral deposition are discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Piez K, Eigner E, Lewis M (1963) The chromatographic separation and amino acid composition of the subunits of several collagens. Biochemistry 1:58–66

    Article  Google Scholar 

  2. Veis A (1985) Molecular structure and models of collagen fibril assembly. In: Reddi AH (ed) Extracellular matrix structure and function. Alan R Liss, New York, pp. 351–358

    Google Scholar 

  3. Hodge AJ, Petruska JA (1963) Recent studies with the electron microscope on ordered aggregates of the tropocollagen macromolecule. In: Ramachandran GN (ed) Aspects of protein structure. Academic Press, New York, pp 289–300

    Google Scholar 

  4. Hulmes KJS, Miller A, Parry DAD, Piez KA, Woodhead-Galloway J (1973) Analysis of the primary structure of collagen for the origins of molecular packing. J Mol Biol 79:137–148

    Article  PubMed  CAS  Google Scholar 

  5. Bear RS (1952) The structure of collagen fibrils. Adv Protein Chem 7:69–160

    Article  PubMed  CAS  Google Scholar 

  6. Meek KM, Chapman JA, Hardcastle RA (1979) The staining pattern of collagen fibrils: improved correlation with sequence data. J Biol Chem 254:10710–10714

    PubMed  CAS  Google Scholar 

  7. Tzaphilidou M, Chapman JA, Meek KM (1982) A study of positive staining for electron microscopy using collagen as a model system-I. Staining by phosphotungstate and tungstate ions. Micron 13:119–131

    Google Scholar 

  8. Tzaphilidou M, Chapman JA, Al-Samman MH (1982) A study of positive staining for electron microscopy using collagen as a model system-II. Staining by uranyl ions. Micron 13:133–145

    Google Scholar 

  9. Chapman JA, Hulmes DJS (1984) Electron microscopy of the collagen fibril. In: Ruggeri A, Motta PM (eds) Ultrastructure of the connective tissue matrix. Martinus Nijhoff, Boston, pp. 1–33

    Google Scholar 

  10. Meek KM, Chapman JA (1985) Glutaraldehyde-induced changes in the axially projected fine structure of collagen fibrils. J Mol Biol 185:359–370

    Article  PubMed  CAS  Google Scholar 

  11. White SW, Hulmes DJS, Miller A, Timmins PA (1977) Collagen-mineral axial relationship in calcified turkey leg tendon by x-ray and neutron diffraction. Nature 266:421–425

    Article  PubMed  CAS  Google Scholar 

  12. Berthet-Colominas C, Miller A, White SW (1979) Structural study of the calcifying collagen in turkey leg tendons. J Mol Biol 134:431–445

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  14. 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 

  15. Arsenault AL (1989) A comparative electron microscopic study of apatite crystals in collagen fibrils of rat bone, dentin and calcified turkey leg tendons. Bone Miner 6:165–177

    Article  PubMed  CAS  Google Scholar 

  16. Arsenault AL (in press) Image analysis of collagenassociated mineral distribution in cryogenically prepared turkey leg tendons. Calcif Tissue Int

  17. Highberger JH, Corbett C, Dixit SN, Wing Y, Jerome MS, Kang AH, Gross J (1982) Amino acid sequence of chick skin collagen α1(I)-CB8 and the complete primary structure of the helical portion of the chick skin collagen α1(I) chain. Biochemistry 21:2048–2054

    Article  PubMed  CAS  Google Scholar 

  18. Boedtker H, Finer M, Sirpa A (1985) The structure of the chicken α2 collagen gene. In: Fleischmajer R, Olsen BR, Kuhn K (eds) The biology, chemistry and pathology of collagen? Ann NY Acad Sci 460:85–116

  19. Hofmann H, Fietzek PP, Kuhn K (1978) The role of polar and hydrophobic interactions for the molecular packing of type I collagen: a three-dimensional evaluation of the amino acid sequence. J Mol Biol 125:137–165

    Article  PubMed  CAS  Google Scholar 

  20. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  21. 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 

  22. 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 

  23. Miller A (1984) Collagen: the organic matrix of bone. Phil Trans R Soc Lond B 304:455–477

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Engström A (1966) Apatite-collagen organization in calcified tendon. Exp Cell Res 43:241–245

    Article  PubMed  Google Scholar 

  26. Scott JE, Haigh M (1985) Proteoglycan-type I collagen fibril interactions in bone and non-calcifying connective tissues. Biosci Rep 5:71–81

    Article  PubMed  CAS  Google Scholar 

  27. 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 

  28. Glimcher MJ, Brickley-Parson D, Kossiva D (1979) Phosphoproteins and γ-glutamic acid-containing peptides in calcified turkey tendon: their absence in uncalcified tendon. Calcif Tissue Int 27:281–284

    Article  PubMed  CAS  Google Scholar 

  29. Hauschka PV, Lian JB, Gallop PM (1975) Direct identification of the calcium-binding amino acid γ-carboxyglutamate in mineralized tissue. Proc Natl Acad Sci USA 72:3925–3929

    Article  PubMed  CAS  Google Scholar 

  30. Tanford C (1980) The hydrophobic effect: formation of micelles and biological membranes, 2nd ed. John Wiley and Sons, New York

    Google Scholar 

  31. Hulmes DJS, Holmes DF, Cummings C (1985) Crystalline regions in collagen fibrils. J Mol Biol 184:473–477

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maitland, M.E., Arsenault, A.L. A correlation between the distribution of biological apatite and amino acid sequence of type I collagen. Calcif Tissue Int 48, 341–352 (1991). https://doi.org/10.1007/BF02556154

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02556154

Key words

Navigation