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Cellular Response of Human Bone Marrow Derived Mesenchymal Stem Cells to Titanium Surfaces Implanted with Calcium and Magnesium Ions

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Abstract

Surface characteristics and cellular response to titanium surfaces that had been implanted with calcium and magnesium ions using plasma immersion ion implantation and deposition (PIIID) were evaluated. Three different titanium surfaces were analyzed: a resorbable blast media (RBM) surface (blasted with hydroxyapatite grit), a calcium ion-implanted surface, and a magnesium ion-implanted surface. The surface characteristics were investigated by scanning electron microscopy (SEM), surface roughness testing, X-ray diffraction (XRD), and Auger electron spectroscopy (AES). Human bone marrow derived mesenchymal stem cells were cultured on the 3 different surfaces. Initial cell attachment was evaluated by SEM, and cell proliferation was determined using MTT assay. Real-time polymerase chain reaction (PCR) was used to quantify osteoblastic gene expression (i.e., genes encoding RUNX2, type I collagen, alkaline phosphatase, and osteocalcin). Surface analysis did not reveal any changes in surface topography after ion implantation. AES revealed that magnesium ions were present in deeper layers than calcium ions. The calcium ion- and magnesium ion-implanted surfaces showed greater initial cell attachment. Investigation of cell proliferation revealed no significant difference among the groups. After 6 days of cultivation, the expression of RUNX2 was higher in the magnesium ion-implanted surface and the expression of osteocalcin was lower in the calcium ion-implanted surface. In conclusion, ion implantation using the PIIID technique changed the surface chemistry without changing the topography. Calcium ion- and magnesium ion-implanted surfaces showed greater initial cellular attachment.

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References

  1. Schwartz Z, Boyan B. Underlying mechanisms at the bone–biomaterial interface. J Cell Biochem. 1994;56:340–7.

    Article  PubMed  CAS  Google Scholar 

  2. Wennerberg A, Albrektsson T. Effects of titanium surface topography on bone integration: a systematic review. Clin Oral Implants Res. 2009;20:172–84.

    Article  PubMed  Google Scholar 

  3. Manso M, Langlet M, Martınez-Duart J. Testing sol–gel CaTiO3 coatings for biocompatible applications. Mater Sci Eng C Mater Biol Appl. 2003;23:447–50.

    Article  CAS  Google Scholar 

  4. Kim H, Miyaji F, Kokubo T, Nakamura T. Preparation of bioactive Ti and its alloys via simple chemical surface treatment. J Biomed Mater Res. 1996;32:409–17.

    Article  PubMed  CAS  Google Scholar 

  5. Sul Y, Johansson CB, Röser K, Albrektsson T. Qualitative and quantitative observations of bone tissue reactions to anodised implants. Biomaterials. 2002;23:1809–17.

    Article  PubMed  CAS  Google Scholar 

  6. Hanawa T, Kamiura Y, Yamamoto S, et al. Early bone formation around calcium-ion-implanted titanium inserted into rat tibia. J Biomed Mater Res. 1997;36:131–6.

    Article  PubMed  CAS  Google Scholar 

  7. Sul Y, Byon EE, Jeong YY. Biomechanical measurements of Calcium-Incorporated oxidized implants in rabbit bone: effect of calcium surface chemistry of a novel implant. Clin Implant Dent Relat Res. 2004;6:101–10.

    Article  PubMed  Google Scholar 

  8. Mändl S, Krause D, Thorwarth G, et al. Plasma immersion ion implantation treatment of medical implants. Surf Coat Technol. 2001;142:1046–50.

    Article  Google Scholar 

  9. Anders A. Handbook of plasma immersion ion implantation and deposition, vol. 8. New York: Wiley; 2000.

    Google Scholar 

  10. Byon E, Moon S, Cho S, Jeong C, Jeong Y, Sul Y. Electrochemical property and apatite formation of metal ion implanted titanium for medical implants. Surf Coat Technol. 2005;200:1018–21.

    Article  CAS  Google Scholar 

  11. Ellingsen JE, Johansson CB, Wennerberg A, Holmen A. Improved retention and bone-to-implant contact with fluoride-modified titanium implants. Int J Oral Maxillofac Implants. 2004;19:659–66.

    PubMed  Google Scholar 

  12. Sul Y, Johansson CB, Kang Y, Jeon D, Albrektsson T. Bone reactions to oxidized titanium implants with electrochemical anion sulphuric acid and phosphoric acid incorporation. Clin Implant Dent Relat Res. 2002;4:78–87.

    Article  PubMed  Google Scholar 

  13. Park J, Suh J, Chung H. Effects of calcium ion incorporation on osteoblast gene expression in MC3T3-E1 cells cultured on microstructured titanium surfaces. J Biomed Mater Res A. 2008;86:117–26.

    Article  PubMed  CAS  Google Scholar 

  14. Nayab S, Jones F, Olsen I. Human alveolar bone cell adhesion and growth on ion-implanted titanium. J Biomed Mater Res A. 2004;69:651–7.

    Article  PubMed  CAS  Google Scholar 

  15. Nayab SN, Jones FH, Olsen I. Effects of calcium ion implantation on human bone cell interaction with titanium. Biomaterials. 2005;26:4717–27.

    Article  PubMed  CAS  Google Scholar 

  16. Sul Y, Johansson P, Chang B, Byon E, Jeong Y. Bone tissue responses to mg-incorporated oxidized implants and machine-turned implants in the rabbit femur. J Appl Biomater Biomech. 2005;3:18–28.

    PubMed  CAS  Google Scholar 

  17. Sul YT, Johansson C, Albrektsson T. Which surface properties enhance bone response to implants? Comparison of oxidized magnesium, TiUnite, and osseotite implant surfaces. Int J Prosthodont. 2006;19:319–28.

    PubMed  Google Scholar 

  18. Cho L, Kim D, Kim J, Byon E, Jeong Y, Park C. Bone response of mg ion-implanted clinical implants with the plasma source ion implantation method. Clin Oral Implants Res. 2010;21:848–56.

    PubMed  Google Scholar 

  19. Park J, Kim Y, Jang J, Song H. Osteoblast response to magnesium ion-incorporated nanoporous titanium oxide surfaces. Clin Oral Implants Res. 2010;21:1278–87.

    Article  PubMed  Google Scholar 

  20. Song W, Heo J, Lee J, Park Y, Kim Y. Osseointegration of magnesium-incorporated sand-blasted acid-etched implant in the dog mandible: resonance frequency measurements and histomorphometric analysis. Tissue Eng Regen Med. 2016;13:191–9.

    Article  CAS  Google Scholar 

  21. Hanawa T, Ukai H, Murakami K. X-ray photoelectron spectroscopy of calcium-ion-implanted titanium. J Electron Spectrosc Relat Phenom. 1993;63:347–54.

    Article  CAS  Google Scholar 

  22. Parise LV, Phillips DR. Fibronectin-binding properties of the purified platelet glycoprotein IIb–IIIa complex. J Biol Chem. 1986;261:14011–7.

    PubMed  CAS  Google Scholar 

  23. Mould AP, Akiyama SK, Humphries MJ. Regulation of integrin α5β1-fibronectin interactions by divalent cations evidence for distinct classes of binding sites for Mn2+, Mg2+, and Ca2+. J Biol Chem. 1995;270:26270–7.

    Article  PubMed  CAS  Google Scholar 

  24. Krause A, Cowles EA, Gronowicz G. Integrin-mediated signaling in osteoblasts on titanium implant materials. J Biomed Mater Res. 2000;52:738–47.

    Article  PubMed  CAS  Google Scholar 

  25. Zreiqat H, Howlett C, Zannettino A, et al. Mechanisms of magnesium-stimulated adhesion of osteoblastic cells to commonly used orthopaedic implants. J Biomed Mater Res. 2002;62:175–84.

    Article  PubMed  CAS  Google Scholar 

  26. Cooper LF, Masuda T, Whitson SW, Yliheikkila P, Felton DA. Formation of mineralizing osteoblast cultures on machined, titanium oxide grit-blasted, and plasma-sprayed titanium surfaces. Int J Oral Maxillofac Implants. 1999;14:37–47.

    PubMed  CAS  Google Scholar 

  27. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641–50.

    Article  PubMed  CAS  Google Scholar 

  28. Wang C, Zhao B, Ai H, Wang Y. Comparison of biological characteristics of mesenchymal stem cells grown on two different titanium implant surfaces. Biomed Mater. 2008;3:015004.

    Article  PubMed  CAS  Google Scholar 

  29. Kassem M. Mesenchymal stem cells: biological characteristics and potential clinical applications. Cloning Stem Cells. 2004;6:369–74.

    Article  PubMed  CAS  Google Scholar 

  30. Cecchinato F, Xue Y, Karlsson J, et al. In vitro evaluation of human fetal osteoblast response to magnesium loaded mesoporous TiO2 coating. J Biomed Mater Res A. 2014;102:3862–71.

    Article  PubMed  CAS  Google Scholar 

  31. Kim B, Kim JS, Park YM, Choi B, Lee J. Mg ion implantation on SLA-treated titanium surface and its effects on the behavior of mesenchymal stem cell. Mater Sci Eng C. 2013;33:1554–60.

    Article  CAS  Google Scholar 

  32. Cheng M, Qiao Y, Wang Q, et al. Calcium plasma implanted titanium surface with hierarchical microstructure for improving the bone formation. ACS Appl Mater Interfaces. 2015;7:13053–61.

    Article  PubMed  CAS  Google Scholar 

  33. Le Guéhennec L, Soueidan A, Layrolle P, Amouriq Y. Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater. 2007;23:844–54.

    Article  PubMed  CAS  Google Scholar 

  34. Albrektsson T, Wennerberg A. Oral implant surfaces: part 1—review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. Int J Prosthodont. 2004;17:536–43.

    PubMed  Google Scholar 

  35. Albrektsson T, Wennerberg A. The impact of oral implants-past and future, 1966–2042. J Can Dent Assoc. 2005;71:327.

    PubMed  Google Scholar 

  36. Lausmaa J. Surface spectroscopic characterization of titanium implant materials. J Electron Spectrosc Related Phenom. 1996;81:343–61.

    Article  CAS  Google Scholar 

  37. Gittens RA, Olivares-Navarrete R, Cheng A, et al. The roles of titanium surface micro/nanotopography and wettability on the differential response of human osteoblast lineage cells. Acta Biomater. 2013;9:6268–77.

    Article  PubMed  CAS  Google Scholar 

  38. Thalji G, Cooper LF. Molecular assessment of osseointegration in vivo: a review of the current literature. Int J Oral Maxillofac Implants. 2013;28:e521–34.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the research fund of Gangneung-Wonju National University (2014100126).

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Correspondence to Chan-Jin Park.

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Won, S., Huh, YH., Cho, LR. et al. Cellular Response of Human Bone Marrow Derived Mesenchymal Stem Cells to Titanium Surfaces Implanted with Calcium and Magnesium Ions. Tissue Eng Regen Med 14, 123–131 (2017). https://doi.org/10.1007/s13770-017-0028-3

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  • DOI: https://doi.org/10.1007/s13770-017-0028-3

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