Skip to main content

Advertisement

Log in

Age-Related Changes in Collagen Properties and Mineralization in Cancellous and Cortical Bone in the Porcine Mandibular Condyle

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

An Erratum to this article was published on 15 February 2011

Abstract

Collagen is an important constituent of bone, and it has been suggested that changes in collagen and mineral properties of bone are interrelated during growth. The aim of this study was to quantify age-related changes in collagen properties and the degree of mineralization of bone (DMB). The DMB in cancellous and cortical bone samples from the mandibular condyle of 35 female pigs aged 0–100 weeks was determined using micro-computed tomography. Subsequently, the amount of collagen and the number of pentosidine (Pen), hydroxylysylpyridinoline (HP), and lysylpyridinoline (LP) cross-links were quantified by means of high-performance liquid chromatography. The amount of collagen increased with age in cancellous bone but remained unchanged in cortical bone. The number of Pen and LP cross-links decreased in both bone types. In contrast, the number of HP cross-links decreased only in cancellous bone. The sum of the number of HP and LP cross-links decreased with age in cancellous bone only. The DMB increased in cancellous and cortical bone. It was concluded that the largest changes in the number of mature collagen cross-links and the mineralization in porcine cancellous and cortical bone take place before the age of 40 weeks. The low number of mature cross-links after this age suggests that the bone turnover rate continues to be high and thereby prevents the development of mature cross-links.

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

Similar content being viewed by others

References

  1. Glimcher MJ (1976) The composition, structure and organization of bone and other mineralized tissues and the mechanisms of calcification. In: Greep RO, Astwood EB (eds) Handbook of physiology: endocrinology, vol 7. American Physiological Society, Washington DC, pp 25–116

    Google Scholar 

  2. Landis WJ, Silver FH (2009) Mineral deposition in the extracellular matrices of vertebrate tissues: identification of possible apatite nucleation sites on type I collagen. Cells Tissues Organs 189:20–24

    Article  CAS  PubMed  Google Scholar 

  3. Pokharna HK, Phillips FM (1998) Collagen crosslinks in human lumbar intervertebral disc aging. Spine 23:1645–1648

    Article  CAS  PubMed  Google Scholar 

  4. Sell DR, Monnier VM (1989) Structure elucidation of a senescence cross-link from human extracellular matrix. J Biol Chem 36:21597–21602

    Google Scholar 

  5. Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7

    Article  PubMed  Google Scholar 

  6. Nyman JS, Roy A, Tyler JH, Acuna RL, Gayle HJ, Wang X (2007) Age-related factors affecting the postyield energy dissipation of human cortical bone. J Orthop Res 25:646–655

    Article  PubMed  Google Scholar 

  7. Van Deemter M, Ponsioen TL, Bank RA, Snabel JM, Van der Worp RJ, Hooymans JM, Los LI (2009) Pentosidine accumulates in the aging vitreous body: a gender effect. Exp Eye Res 88:1043–1050

    Article  PubMed  Google Scholar 

  8. Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A (2005) Advanced glycation end products and bone loss during aging. Ann NY Acad Sci 1043:710–717

    Article  CAS  PubMed  Google Scholar 

  9. Fraser WD (1998) The collagen cross-links pyridinoline and deoxypyrodinoline: a review of their biochemistry, physiology, measurement, and clinical applications. J Clin Lig Assay 2:102–110

    Google Scholar 

  10. Delmas PD, Schlemmer A, Gineyts E, Riis B, Christiansen C (1991) Urinary excretion of pyridinoline crosslinks correlates with bone turnover measured on iliac crest biopsy in patients with vertebral osteoporosis. J Bone Miner Res 6:639–643

    Article  CAS  PubMed  Google Scholar 

  11. Shaw NJ, Dutton J, Fraser WD, Smith CS (1995) Urinary pyridinoline and deoxypyridinoline excretion in children. Clin Endocrinol (Oxf) 42:607–612

    Article  CAS  Google Scholar 

  12. Açil Y, Brinckmann J, Notbohm H, Müller PK, Bätge B (1996) Changes with age in the urinary excretion of hydroxylysylpyridinoline (HP) and lysylpyridinoline (LP). Scand J Clin Lab Invest 56:275–283

    Article  PubMed  Google Scholar 

  13. Tsukahara H, Miura M, Hori C, Hiraoka M, Nosaka K, Hata K, Konishi Y, Sudo M (1996) Urinary excretion of pyridinium cross-links of collagen in infancy. Metabolism 45:510–514

    Article  CAS  PubMed  Google Scholar 

  14. Mora S, Prinster C, Proverbio MC, Bellini A, De Poli SC, Weber G, Abbiati G, Chiumello G (1998) Urinary markers of bone turnover in healthy children and adolescents: age-related changes and effect of puberty. Calcif Tissue Int 63:369–374

    Article  CAS  PubMed  Google Scholar 

  15. Kraenzlin ME, Kraenzlin CA, Meier C, Giunta C, Steinmann B (2008) Automated HPLC assay for urinary collagen cross-links: effect of age, menopause, and metabolic bone diseases. Clin Chem 54:1546–1553

    Article  CAS  PubMed  Google Scholar 

  16. Willems NMBK, Mulder L, Langenbach GEJ, Grünheid T, Zentner A, Van Eijden TMGJ (2007) Age-related changes in microarchitecture and mineralization of cancellous bone in the porcine mandibular condyle. J Struct Biol 158:421–427

    Article  CAS  PubMed  Google Scholar 

  17. Mulder L, Koolstra JH, Weijs WA, Van Eijden TMGJ (2005) Architecture and mineralization of developing trabecular bone in the pig mandibular condyle. Anat Rec A Discov Mol Cell Evol Biol 285:659–666

    PubMed  Google Scholar 

  18. Jee WSS (1999) Structure and function of bone tissue. In: Bronner F, Worrell RV (eds) Orthopedics, principles of basic and clinical science, vol 3. CRC Press, Boca Raton, pp 3–28

    Google Scholar 

  19. Herring SW (2003) TMJ anatomy and animal models. J Musculoskelet Neuronal Interact 3(91–94):406–407

    Google Scholar 

  20. Mulder L, Koolstra JH, Van Eijden TMGJ (2004) Accuracy of microCT in the quantitative determination of the degree and distribution of mineralization in developing bone. Acta Radiol 45:769–777

    Article  CAS  PubMed  Google Scholar 

  21. Bank RA, Jansen EJ, Beekman B, TeKoppele JM (1996) Amino acid analysis by reverse-phase high-performance liquid chromatography: improved derivatization and detection conditions with 9-fluorenylmethyl chloroformate. Anal Biochem 240:167–176

    Article  CAS  PubMed  Google Scholar 

  22. Bank RA, Beekman B, Verzijl N, De Roos JADM, Sakkee AN, TeKoppele JM (1997) Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J Chromatogr B 703:37–44

    Article  CAS  Google Scholar 

  23. Shikata H, Hiramatsu M, Masumizu T, Fujimoto D, Utsumi N (1985) Age-related changes in the content of non-reducible crosslinks in rat mandibular bone. Arch Oral Biol 30:451–453

    Article  CAS  PubMed  Google Scholar 

  24. Eyre DR, Dickson IR, Van Ness K (1988) Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J 252:495–500

    CAS  PubMed  Google Scholar 

  25. Rath NC, Balog JM, Huff WE, Huff G, Kulkarni GB, Tierce JF (1999) Comparative differences in the composition and biomechanical properties of tibiae of seven- and seventy-two-week-old male and female broiler breeder chickens. Poult Sci 78:1232–1239

    CAS  PubMed  Google Scholar 

  26. Nyman JS, Roy A, Acuna RL, Gayle HJ, Reyes MJ, Tyler JH, Dean DD, Wang X (2006) Age-related effect on the concentration of collagen crosslinks in human osteonal and interstitial bone tissue. Bone 39:1210–1217

    Article  CAS  PubMed  Google Scholar 

  27. Oxlund H, Mosekilde L, Ørtoft G (1996) Reduced concentration of collagen reducible cross links in human trabecular bone with respect to age and osteoporosis. Bone 19:479–484

    Article  CAS  PubMed  Google Scholar 

  28. Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L (1999) Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int 65:203–210

    Article  CAS  PubMed  Google Scholar 

  29. Zioupos P, Currey JD, Hamer AJ (1999) The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res 45:108–116

    Article  CAS  PubMed  Google Scholar 

  30. Landis WJ, Paine MC, Hodgens KJ, Glimcher MJ (1986) Matrix vesicles in embryonic chick bone: considerations of their identification, number, distribution, and possible effects on calcification of extracellular matrices. J Ultrastruct Mol Struct Res 95:142–163

    Article  CAS  PubMed  Google Scholar 

  31. Knott L, Bailey AJ (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22:181–187

    Article  CAS  PubMed  Google Scholar 

  32. Jee WSS (2001) Integrated bone tissue physiology: anatomy and physiology. In: Cowin SC (ed) Bone mechanics handbook, vol 1, 2nd edn. CRC Press, Boca Raton, pp 1–68

    Google Scholar 

  33. Grandhee SK, Monnier VM (1991) Mechanism of formation of the Maillard protein cross-link pentosidine. Glucose, fructose, and ascorbate as pentosidine precursors. J Biol Chem 266:11649–11653

    CAS  PubMed  Google Scholar 

  34. Teng S, Herring SW (1995) A stereological study of trabecular architecture in the mandibular condyle of the pig. Arch Oral Biol 40:299–310

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nop M. B. K. Willems.

Additional information

The authors have stated that they have no conflict of interest.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00223-011-9469-1

Electronic supplementary material

Below is the link to the electronic supplementary material.

223_2010_9339_MOESM1_ESM.eps

Supplementary material 1 Frontal view of a mandibular condyle (transparent). Cancellous and cortical bone samples were obtained near the center and near the surface of the condyle, respectively. The distribution of the mineral in the samples is shown. Scale: the degree of mineralization of bone (DMB) increases from green to red. Please note this is a left condyle.(EPS 639 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Willems, N.M.B.K., Langenbach, G.E.J., Everts, V. et al. Age-Related Changes in Collagen Properties and Mineralization in Cancellous and Cortical Bone in the Porcine Mandibular Condyle. Calcif Tissue Int 86, 307–312 (2010). https://doi.org/10.1007/s00223-010-9339-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-010-9339-2

Keywords

Navigation