Skip to main content

Advertisement

SpringerLink
Log in

Glucuronic acid and phosphoserine act as mineralization mediators of collagen I based biomimetic substrates

  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Glucuronic acid (GlcA) and phosphoserine (pS) carrying acidic functional groups were used as model molecules for glycosaminoglycans and phosphoproteins, respectively to mimic effects of native biomolecules and influence the mineralization behaviour of collagen I. Collagen substrates modified with GlcA showed a stable interaction between GlcA and collagen fibrils. Substrates were mineralized using the electrochemically assisted deposition (ECAD) in a Ca2+/H x PO (3−x)4 electrolyte at physiological pH and temperature. During mineralization of collagen–GlcA matrices, crystalline hydroxyapatite (HA) formed earlier with increasing GlcA content of the collagen matrix, while the addition of pS to the electrolyte succeeded in inhibiting the transformation of preformed amorphous calcium phosphate (ACP) to HA. The lower density of the resulting mineralization and the coalesced aggregates formed at a certain pS concentration suggest an interaction between calcium and the phosphate groups of pS involving the formation of complexes. Combining GlcA-modified collagen and pS-modified electrolyte showed dose-dependent cooperative effects.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. De Jonge LT, Leeuwenburgh SCG, Wolke JGC, Jansen JA. Organic–inorganic surface modifications for titanium implant surfaces. Pharm Res. 2008;25(10):2357–69.

    Article  CAS  PubMed  Google Scholar 

  2. Rössler S, Born R, Scharnweber D, Worch H, Sewing A, Dard M. Biomimetic coatings functionalized with adhesion peptides for dental implants. J Mater Sci Mater Med. 2001;12:871–7.

    Article  Google Scholar 

  3. Bierbaum S, Douglas T, Hanke T, Scharnweber D, Tippelt S, Monsees T, et al. Collageneous matrix coatings on titanium implants modified with decorin and chondroitin sulfate: characterization and influence on osteoblastic cells. J Biomed Mater Res A. 2006;77:551–62.

    PubMed  Google Scholar 

  4. Morra M. Biochemical modification of titanium surfaces: peptides and ECM proteins. Eur Cell Mater. 2006;12:1–15.

    CAS  PubMed  ADS  Google Scholar 

  5. Jäger I, Fratzl P. Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J. 2000;79(4):1737–46.

    Article  PubMed  Google Scholar 

  6. Mann S. Biomineralization. Principles and concepts in bioinorganic materials chemistry. Oxford University Press; 2001.

  7. Boskey AL. Matrix proteins and mineralization: an overview. Connect Tissue Res. 1996;35:357–63.

    Article  CAS  PubMed  Google Scholar 

  8. Schliephake H, Scharnweber D, Rössler S, Dard M, Sewing A, Aref A. Biomimetic calcium phosphate composite coating of dental implants. Int J Oral Maxillofac Implants. 2006;21:738–46.

    PubMed  Google Scholar 

  9. Wuttke M, Müller S, Nitsche DP, Paulsson M, Hanisch FG, Maurer P. Structural characterization of human recombinant and bone-derived bone sialoprotein. Functional implications for cell attachment and hydroxyapatite binding. J Biol Chem. 2001;276:36839–48.

    Article  CAS  PubMed  Google Scholar 

  10. Hunter GK, Goldberg HA. Modulation of crystal formation by bone phosphoproteins: role of glutamic acid-rich sequences in the nucleation of hydroxyapatite by bone sialoprotein. Biochem J. 1994;302:175–9.

    CAS  PubMed  Google Scholar 

  11. Hunter GK, Kyle CL, Goldberg HA. Modulation of crystal formation by bone phosphoproteins: structural specificity of the osteopontin-mediated inhibition of hydroxyapatite formation. Biochem J. 1994;300:723–8.

    CAS  PubMed  Google Scholar 

  12. Paschalakis P, Vynios DH, Tsiganos CP, Dalas E, Maniatis C, Koutsoukos PG. Effect of proteoglycans on hydroxyapatite growth in vitro: the role of hyaluronan. Biochim Biophys Acta. 1993;1158:129–36.

    CAS  PubMed  Google Scholar 

  13. Waddington RJ, Hall RC, Embery G, Lloyd DM. Changing profiles of proteoglycans in the transition of predentine to dentine. Matrix Biol. 2003;22:153–61.

    Article  CAS  PubMed  Google Scholar 

  14. Paschalakis P, Vynios DH, Tsiganos CP, Koutsoukos PG. Inhibition of hydroxyapatite in vitro by glucosaminoglycans: the effect of size, sulphation and primary structure, in water soluble polymers, solution properties and applications. In: Amjad Z ed. New York: Plenum Press; 1998. P. 63–75.

  15. Iozzo RV. The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J Biol Chem. 1999;274:18843–6.

    Article  CAS  PubMed  Google Scholar 

  16. Keene DR, Antonio JDS, Mayne R, McQuillan DJ, Sarris G, Santoro SA, et al. Decorin binds near the C terminus of type I collagen. J Biol Chem. 2000;275:21801–4.

    Article  CAS  PubMed  Google Scholar 

  17. Hunter GK, Poitras MS, Underhill TM, Grynpas MD, Goldberg HA. Induction of collagen mineralization by a bone sialoprotein-decorin chimeric protein. J Biomed Mater Res. 2001;55:496–502.

    Article  CAS  PubMed  Google Scholar 

  18. Goldoni S, Owens RT, McQuillan DJ, Shriver Z, Sasisekharan R, Birk DE, et al. Biologically active decorin is a monomer in solution. J Biol Chem. 2004;279:6606–12.

    Article  CAS  PubMed  Google Scholar 

  19. Ding A, Ojingwa JC, McDonagh AF, Burlingame AL, Benet LZ. Evidence for covalent binding of acyl glucuronides to serum albumin via an imine mechanism as revealed by tandem mass spectrometry. Proc Natl Acad Sci. 1993;90:3797–801.

    Article  CAS  PubMed  ADS  Google Scholar 

  20. Casu B. Structural features and binding properties of chondroitin sulfates, dermatan sulfate, and heparan sulfate. Semin Thromb Hemost, Istituto di Chimica e Biochimica G. Ronzoni, Milan, Italy. 1991;17:9–14.

    Google Scholar 

  21. Vogel KG, Trotter JA. The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Coll Relat Res. 1987;7:105–14.

    CAS  PubMed  Google Scholar 

  22. Aoba T, Moreno EC. Adsorption of phosphoserine onto hydroxyapatite and its inhibitory activity on crystal growth. J Colloid Interface Sci. 1985;106:110–21.

    Article  CAS  Google Scholar 

  23. Misra DN. Interaction of ortho-phospho-l-serine with hydroxyapatite: formation of a surface complex. J Colloid Interface Sci. 1997;194:249–55.

    Article  CAS  PubMed  Google Scholar 

  24. Reinstorf A, Ruhnow M, Gelinsky M, Pompe W, Hempel U, Wenzel KW, et al. Phosphoserine - a convenient compound for modification of calcium phosphate bone cement collagen composites. J Mater Sci Mater Med. 2004;15:451–5.

    Article  CAS  PubMed  Google Scholar 

  25. Leon B, Jansen JA. Thin calcium phosphate coatings for medical implants. Springer; 2008.

  26. Rössler S, Sewing A, Stölzel M, Born R, Scharnweber D, Dard M, et al. Electrochemically assisted deposition of thin calcium phosphate coatings at near-physiological pH and temperature. J Biomed Mater Res A. 2003;64:655–63.

    Article  PubMed  Google Scholar 

  27. Sewing A, Lakatos M, Scharnweber D, Rössler S, Born R, Dard M, et al. Influence of Ca/P ratio on electrochemical assisted deposition of HAP on titanium. Key Eng Mater. 2004;254–256:419–22.

    Article  Google Scholar 

  28. Lowry O, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265–75.

    CAS  PubMed  Google Scholar 

  29. Mecozzi M, Dragone P, Amici M, Pietrantonio E. Ultrasound assisted extraction and determination of the carbohydrate fraction in marine sediments. Org Geochem. 2000;31:1797–803.

    Article  CAS  Google Scholar 

  30. Rey C, Combes C, Drouet C, Lebugle A, Sfihi H, Barroug A. Nanocrystalline apatites in biological systems: characterization, structure and properties. Mat-wiss u Werkstofftech. 2007;38(12):996–1002.

    Article  CAS  Google Scholar 

  31. Koutsopoulos S. Synthesis and characterization of hydroxyapatite crystals: a review study on the analytical methods. J Biomed Mater Res. 2002;62:600–12.

    Article  CAS  PubMed  Google Scholar 

  32. Combes C, Rey C, Mounic S. Identification and evaluation of HPO4 ions in biomimetic poorly crystalline apatite and bone mineral. Key Eng Mater. 2001;192–5:143–6.

    Article  Google Scholar 

  33. Birk DE, Lande MA. Corneal and scleral collagen fiber formation in vitro. Biochim Biophys Acta. 1981;670:362–9.

    CAS  PubMed  Google Scholar 

  34. Iberg N, Flückiger R. Nonenzymatic glycosylation of albumin in vivo. Identification of multiple glycosylated sites. J Biol Chem. 1986;261:13542–5.

    CAS  PubMed  Google Scholar 

  35. Garlick R, Mazer J. The principal site of nonenzymatic glycosylation of human serum albumin in vivo. J Biol Chem. 1983;258:6142–6.

    CAS  PubMed  Google Scholar 

  36. Born R, Scharnweber D, Rössler S, Stölzel M, Thieme M, Wolf C, et al. Surface analysis of titanium based biomaterials. Fresenius J anal Chem. 1998;361:697–700.

    Article  CAS  Google Scholar 

  37. Elliot JC. Structure and chemistry of the apatites and other calcium orthophosphates. 2nd ed. Amsterdam: Elsevier; 1994. p 58–60, 259–63.

  38. Posner A, Blumethal NC, Betts F. Chemistry and structure of precipitated hydroxyapatites. In: Nriagu JO, Moore PB, editors. Phosphate minerals. Berlin/Heidelberg: Springer Verlag; 1984. p. 155–71.

    Google Scholar 

  39. Lowenstam HA, Weiner S. On biomineralization. New York: Oxford University Press; 1989.

    Google Scholar 

  40. Crane NJ, Popescu V, Morris MD, Steenhuis P, Ignelzi MA Jr. Raman spectroscopic evidence for octacalcium phosphate and other transient mineral species deposited during intramembranous mineralization. Bone. 2006;39:434–42.

    Article  CAS  PubMed  Google Scholar 

  41. Weiner S. Transient precursor strategy in mineral formation of bone. Bone. 2006;39:431–3.

    Article  CAS  PubMed  Google Scholar 

  42. Mahamid J, Sharir A, Addadi L, Weiner S. Amorphous calcium phosphate is a major component of the forming fin bones of zebrafish: indications for an amorphous precursor phase. Proc Natl Acad Sci USA. 2008;105:12748–53.

    Article  CAS  PubMed  ADS  Google Scholar 

  43. Rey C, Simizu M, Collins B, Glimcher MJ. Resolution-enhanced Fourier transform infrared spectroscopy study for the environment of phosphate ion in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age: 2. Investigations in the ν3 PO4 domain. Calcif Tissue Int. 1991;49:383–8.

    Article  CAS  PubMed  Google Scholar 

  44. Jäger C, Welzel T, Meyer-Zaika W, Epple M. A solid-state NMR investigation of the structure of nanocrystalline hydroxyapatite. Magn Reson Chem. 2006;44:573–80.

    Article  PubMed  Google Scholar 

  45. Grynpas MD. Transient precursor strategy or very small biological apatite crystals? Bone. 2007;41:162–4.

    Article  CAS  PubMed  Google Scholar 

  46. Scharnweber D, Born R, Flade K, Rössler S, Stölzel M, Worch H. Mineralization behaviour of collagen type I immobilized on different substrates. Biomaterials. 2004;25:2371–80.

    Article  CAS  PubMed  Google Scholar 

  47. Linde A, Lussi A, Crenshaw MA. Mineral induction by immobilized polyanionic proteins. Calcif Tissue Int. 1989;44:286–95.

    Article  CAS  PubMed  Google Scholar 

  48. Addadi L, Weiner S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci USA. 1985;82:4110–4.

    Article  CAS  PubMed  ADS  Google Scholar 

  49. Addadi L, Moradian J, Shay E, Maroudas NG, Weiner S. A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: relevance to biomineralization. Proc Natl Acad Sci USA. 1987;82:2732–6.

    Article  ADS  Google Scholar 

  50. Van den Bos T, Beertsen WJ. Bound phosphoproteins enhance mineralization of alkaline phosphatase-collagen complexes in vivo. Bone Miner Res. 1994;9:1205–9.

    Article  CAS  Google Scholar 

  51. Glimcher MJ. Mechanism of calcification: role of collagen fibrils and collagen-phosphoprotein complexes in vitro and in vivo. Anat Rec. 1989;224:139–53.

    Article  CAS  PubMed  Google Scholar 

  52. Benaziz L, Barroug A, Legrouri A, Rey C, Lebugle A. Adsorption of o-phospho-l-serine and l-serine onto poorly crystalline apatite. J Colloid Interface Sci. 2001;238:48–53.

    Article  CAS  PubMed  Google Scholar 

  53. Glimcher MJ. Disorders of bone and mineral metabolism. In: Fredric LC, Murray JF, editors. New York: Raven Press; 1992. P. 26.

Download references

Acknowledgements

The authors thank: Sophie Rössler, Thomas Hanke and Klaus Becker for their technical assistance and helpful discussions.

Author information

Authors and Affiliations

  1. Max Bergmann Center of Biomaterials, Dresden University of Technology, Budapester Str. 27, 01069, Dresden, Germany

    Ricardo Tejero, Susanne Bierbaum, Timothy Douglas, Antje Reinstorf, Hartmut Worch & Dieter Scharnweber

Authors
  1. Ricardo Tejero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susanne Bierbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy Douglas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antje Reinstorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hartmut Worch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dieter Scharnweber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ricardo Tejero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tejero, R., Bierbaum, S., Douglas, T. et al. Glucuronic acid and phosphoserine act as mineralization mediators of collagen I based biomimetic substrates. J Mater Sci: Mater Med 21, 407–418 (2010). https://doi.org/10.1007/s10856-009-3879-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10856-009-3879-x

Keywords

Search

Navigation