Skip to main content

Advertisement

Log in

Computational segmentation of collagen fibers in bone matrix indicates bone quality in ovariectomized rat spine

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Bone loss varies according to disease and age and these variations affect bone cells and extracellular matrix. Osteoporosis rat models are widely investigated to assess mechanical and structural properties of bone; however, bone matrix proteins and their discrepant regulation of diseased and aged bone are often overlooked. The current study considered the spine matrix properties of ovariectomized rats (OVX) against control rats (Sham) at 16 months of age. Diseased bone showed less compact structure with inhomogeneous distribution of type 1 collagen (Col1) and changes in osteocyte morphology. Intriguingly, demineralization patches were noticed in the vicinity of blood vessels in the OVX spine. The organic matrix structure was investigated using computational segmentation of collagen fibril properties. In contrast to the aged bone, diseased bone showed longer fibrils and smaller orientation angles. The study shows the potential of quantifying transmission electron microscopy images to predict the mechanical properties of bone tissue.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. El Khassawna T, Bocker W, Brodsky K, Weisweiler D, Govindarajan P, Kampschulte M, Thormann U, Henss A, Rohnke M, Bauer N, Muller R, Deutsch A, Ignatius A, Durselen L, Langheinrich A, Lips KS, Schnettler R, Heiss C (2015) Impaired extracellular matrix structure resulting from malnutrition in ovariectomized mature rats. Histochem Cell Biol 144:491–507. doi:10.1007/s00418-015-1356-9

    Article  PubMed  Google Scholar 

  2. Boudaoud A, Burian A, Borowska-Wykręt D, Uyttewaal M, Wrzalik R, Kwiatkowska D, Hamant O (2014) FibrilTool, an ImageJ plug-into quantify fibrillar structures in raw microscopy images. Nat Protoc 9:457–463

    Article  CAS  PubMed  Google Scholar 

  3. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykręt D, Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149:439–451

    Article  CAS  PubMed  Google Scholar 

  4. Lucas JR, Shaw SL (2012) MAP65-1 and MAP65-2 promote cell proliferation and axial growth in Arabidopsis roots. Plant J 71:454–463

    CAS  PubMed  Google Scholar 

  5. Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin–myosin network drive apical constriction. Nature 457:495–499

    Article  CAS  PubMed  Google Scholar 

  6. Bredfeldt JS, Liu Y, Pehlke CA, Conklin MW, Szulczewski JM, Inman DR, Keely PJ, Nowak RD, Mackie TR, Eliceiri KW (2014) Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer. J Biomed Opt 19:016007-07

    Article  Google Scholar 

  7. Craig AS, Birtles MJ, Conway JF, Parry DA (1989) An estimate of the mean length of collagen fibrils in rat tail-tendon as a function of age. Connect Tissue Res 19:51–62

    Article  CAS  PubMed  Google Scholar 

  8. Buehler MJ (2006) Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc Natl Acad Sci USA 103:12285–12290. doi:10.1073/pnas.0603216103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Peterlik H, Roschger P, Klaushofer K, Fratzl P (2006) From brittle to ductile fracture of bone. Nat Mater 5:52–55

    Article  CAS  PubMed  Google Scholar 

  10. Kawska A, Hochrein O, Brickmann J, Kniep R, Zahn D (2008) The nucleation mechanism of fluorapatite-collagen composites: ion association and motif control by collagen proteins. Angew Chem Int Ed Engl 47:4982–4985

    Article  CAS  PubMed  Google Scholar 

  11. Cölfen H, Antonietti M (2008) Mesocrystals and nonclassical crystallization. chap 12. Wiley, New Jersey, pp 257–264

  12. Song RQ, Cölfen H (2010) Mesocrystals—ordered nanoparticle superstructures. Adv Mater 22:1301–1330

    Article  CAS  PubMed  Google Scholar 

  13. Tanaka T, Sato H, Doi H, Yoshida CA, Shimizu T, Matsui H, Yamazaki M, Akiyama H, Kawai-Kowase K, Iso T, Komori T, Arai M, Kurabayashi M (2008) Runx2 represses myocardin-mediated differentiation and facilitates osteogenic conversion of vascular smooth muscle cells. Mol Cell Biol 28:1147–1160

    Article  CAS  PubMed  Google Scholar 

  14. Julien M, Khoshniat S, Lacreusette A, Gatius M, Bozec A, Wagner EF, Wittrant Y, Masson M, Weiss P, Beck L, Magne D, Guicheux J (2009) Phosphate-dependent regulation of MGP in osteoblasts: role of ERK1/2 and Fra-1. J Bone Miner Res 24:1856–1868

    Article  CAS  PubMed  Google Scholar 

  15. Murshed M, Schinke T, McKee MD, Karsenty G (2004) Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol 165:625–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gruber HE (1992) Adaptations of Goldner's Masson trichrome stain for the study of undecalcified plastic embedded bone. Biotech Histochem 67(1):30–34

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This is a multicenter study and part of the Collaborating Research Center funding program SFB-/Transregio TRR 79 of the German Research Foundation (DFG) for subprojects T1, Z2, B7, and B12. The authors would also like to thank Annette Stengel, Ida Oberst, and Iris Schulz from Experimental Trauma Surgery (Justus-Liebig University, Giessen, Germany) for their invaluable help and excellent technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thaqif El Khassawna.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 661 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Daghma, D.E.S., Malhan, D., Simon, P. et al. Computational segmentation of collagen fibers in bone matrix indicates bone quality in ovariectomized rat spine. J Bone Miner Metab 36, 297–306 (2018). https://doi.org/10.1007/s00774-017-0844-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-017-0844-5

Keywords

Navigation