Skip to main content
Log in

Influence of Fe3O4 Nanoparticles in Hydroxyapatite Scaffolds on Proliferation of Primary Human Fibroblast Cells

  • Published:
Journal of Materials Engineering and Performance Aims and scope Submit manuscript

Abstract

Modern techniques for expanding stem cells play a substantial role in tissue engineering: the raw material that facilitates regeneration of damaged tissues and treats diseases. The environmental conditions and bioprocessing methods are the primary determinants of the rate of cultured stem cell proliferation. Bioceramic scaffolds made of calcium phosphate are effective substrates for optimal cell proliferation. The present study investigates the effects of two bioceramic scaffolds on proliferating cells in culture media. One scaffold was made of hydroxyapatite and the other was a mixture of hydroxyapatite and ferromagnetic material (Fe3O4 nanoparticles). Disk-shaped (10 mm × 2 mm) samples of the two scaffolds were prepared. Primary human fibroblast proliferation was 1.8- and 2.5-fold faster, respectively, when cultured in the presence of hydroxyapatite or ferrous nanoparticle/hydroxyapatite mixtures. Optical microscopy images revealed that the increased proliferation was due to enhanced cell-cell contact. The presence of magnetic Fe3O4 nanoparticles in the ceramic scaffolds significantly increased cell proliferation compared to hydroxyapatite scaffolds and tissue culture polystyrene.

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
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  1. A.J. Mothe and C.H. Tator, Advances in Stem Cell Therapy for Spinal Cord Injury, J. Clin. Invest., 2012, 122(11), p 3824–3834

    Article  Google Scholar 

  2. F. Berthiaume, T.J. Maguire, and M.L. Yarmush, Tissue Engineering and Regenerative Medicine: History, Progress, and Challenges, Ann. Rev. Chem. Biomol. Eng., 2011, 2, p 403–430

    Article  Google Scholar 

  3. M. Mimeault and S.K. Batra, Concise Review: Recent Advances on the Significance of Stem Cells in Tissue Regeneration and Cancer Therapies, Stem Cells, 2006, 24, p 2319–2345

    Article  Google Scholar 

  4. A.M. Parr, C.H. Tator, and A. Keating, Bone Marrow-Derived Mesenchymal Stromal Cells for the Repair of Central Nervous System Injury, Bone Marrow Transpl., 2007, 40, p 609–619

    Article  Google Scholar 

  5. K.E. Hatzistergos, H. Quevedo, B.N. Oskouei, H. Qinghua, G.S. Feigenbaum, I.S. Margitich, R. Mazhari et al., Bone Marrow Mesenchymal Stem Cells Stimulate Cardiac Stem Cell Proliferation and Differentiation Novelty and Significance, Circ. Res., 2010, 107, p 913–922

    Article  Google Scholar 

  6. M. Körbling and Z. Estrov, Adult Stem Cells for Tissue Repair—A New Therapeutic Concept, N. Engl. J. Med., 2003, 349, p 570–582

    Article  Google Scholar 

  7. C.P. Hodgkinson, J.A. Gomez, M. Mirotsou, and V.J. Dzau, Genetic Engineering of Mesenchymal Stem Cells and its Application in Human Disease Therapy, Hum. Gene Ther., 2010, 21, p 1513–1526

    Article  Google Scholar 

  8. S. Polgar, L. Karimi, and M.E. Morris, Stem Cell Therapy for Parkinson’ s disease: Are Double-Blind Randomized Control Trials the Best Design for Quantifying Therapy Outcomes?, J. Neurol. Neurophysiol., 2013, 4, p 170. doi:10.4172/2155-9562.1000170

    Google Scholar 

  9. I. García-Gómez, G. Elvira, A.G. Zapata, M.L. Lamana, M. Ramírez, J. García Castro, M. García Arranz, A. Vicente, J. Bueren, and D. García-Olmo, Mesenchymal Stem Cells: Biological Properties and Clinical Applications, Expert Opin. Biol. Ther., 2010, 10(10), p 1453–1468

    Article  Google Scholar 

  10. L. Mazzini, K. Mareschi, I. Ferrero, E. Vassallo, G. Oliveri, N. Nasuelli, G.D. Oggioni, L. Testa, and F. Fagioli, Stem Cell Treatment in Amyotrophic Lateral Sclerosis, J. Neurol. Sci., 2008, 265, p 78–83

    Article  Google Scholar 

  11. Y. Ikada, Challenges in Tissue Engineering, J. R. Soc. Interface, 2006, 3, p 589–601

    Article  Google Scholar 

  12. A.D. Ebert and C.N. Svendsen, Human Stem Cells and Drug Screening: Opportunities and Challenges, Nat. Rev. Drug Discov., 2010, 9, p 367–372

    Article  Google Scholar 

  13. Y. Ikada, Tissue Engineering: Fundamentals and Applications, Vol 46, Elsevier, San Diego, 2011

    Google Scholar 

  14. H. Patil, I.S. Chandel, A.K. Rastogi, and P. Srivastava, Studies on a Novel Bioreactor Design for Chondrocyte Culture, International Journal of Tissue Engineering, 2013, 2013, p 1–7

    Article  Google Scholar 

  15. J.E. Hambor, Bioreactor Design and Bioprocess Controls for Industrialized Cell Processing, BioProcess Int., 2012, 10, p 22–33

    Google Scholar 

  16. M. Serra, C. Brito, C. Correia, and P.M. Alves, Process Engineering of Human Pluripotent Stem Cells for Clinical Application, Trends Biotechnol., 2012, 30, p 350–359

    Article  Google Scholar 

  17. A.C. Allori, A.M. Sailon, and S.M. Warren, Biological Basis of Bone Formation, Remodeling, and Repair—Part I: Biochemical Signaling Molecules, Tissue Eng. B, 2008, 14, p 259–273

    Article  Google Scholar 

  18. G.M. Harbers and D.W. Grainger, Cell-Material Interactions: Fundamental Design Issues for Tissue Engineering and Clinical Considerations. An Introduction to Biomaterials, Taylor Francis Group, Boca Raton, FL, 2006, p 15–45

    Google Scholar 

  19. G. Huang, L. Wang, S.Q. Wang, Y. Han, W. Jinhui, Q. Zhang, X. Feng, and T.J. Lu, Engineering Three-Dimensional Cell Mechanical Microenvironment with Hydrogels, Biofabrication, 2012, 4, p 042001

    Article  Google Scholar 

  20. S. Mashayekhan, M. Hajiabbas, and A. Fallah, Stem Cells in Tissue Engineering, 2013, doi:10.5772/54371

  21. T. Mygind, M. Stiehler, A. Baatrup, H. Li, X. Zou, A. Flyvbjerg et al., Mesenchymal Stem Cell Ingrowth and Differentiation on Coralline Hydroxyapatite Scaffolds, Biomaterials, 2007, 28(6), p 1036–1047

    Article  Google Scholar 

  22. D. Turhani, E. Watzinger, M. Weissenbock, B. Cvikl, D. Thurnher, G. Wittwer et al., Analysis of Cell-Seeded 3-Dimensional Bone Constructs Manufactured In Vitro with Hydroxyapatite Granules Obtained from Red Algae, J. Oral Maxillofac. Surg., 2005, 63, p 673–681

    Article  Google Scholar 

  23. F.H. Liu, Fabrication of Bioceramic Bone Scaffolds for Tissue Engineering, J. Mater. Eng. Perform., 2014, 23, p 3762–3769

    Article  Google Scholar 

  24. J.G. Ocampo, M.E. Jaramillo, D.E. Sierra, and C.O. Orozco, Suspension Rheology, Porosity and Mechanical Strength of Porous Hydroxyapatite Obtained by Gel-casting and Infiltration, J. Mater. Eng. Perform., 2016, 25, p 431–442

    Article  Google Scholar 

  25. F. Bistolfi, Radiazioni non ionizzanti, ordine, disordine e biostrutture, Minerva Medica, Torino, 1989, p 209–246

    Google Scholar 

  26. E. Neumann, Membrane Electroporation: Toward a Molecular Mechanism. Electricity and Magnetism in Biology and Medicine, University of Bielefeld, Bielefeld, 1992

    Google Scholar 

  27. Y. Mouneimne, Electroinsertion of Proteins into Membranes: A Novel Approach to the Study of Membrane Receptors, Harvard University, USA. Electricity and Magnetism in Biology and Medicine, University of Bielefeld, San Francisco, 1992

    Google Scholar 

  28. C.E. Lindgren, Capturing the Aura Integrating Science, Technology and Metaphysics, Motilal Banarsidass Publishe, New Delhi, 2008

    Google Scholar 

  29. N. Dekhtyar, N. Polyaka, R. Sammons, 14th Baltic Conference on Biomedical Engineering and Medical Physics, Vol. 20, Springer, Berlin, 2008

  30. D. Kumar, J.P. Gittings, I.G. Turner, C.R. Bowen, A. . Bastida-Hidalgo, and S.H. Cartmell, Polarization of Hydroxyapatite: Influence on Osteoblast Cell Proliferation, Acta Biomater., 2010, 6, p 1549–1554

    Article  Google Scholar 

  31. S. Bodhak, S. Bose, and A. Bandyopadhyay, Bone Cell-Material Interactions on Metal-Ion Doped Polarized Hydroxyapatite, Mater. Sci. Eng., C, 2011, 31, p 755–761

    Article  Google Scholar 

  32. W.R. Adey, Electromagnetics in Biology and Medicine, Modern Radio Science, H. Matsumoto, Ed., Oxford University Press, Oxford, 1993, p 245–277

    Google Scholar 

  33. T.Y. Tsong, Deciphering the Language of Cells, Trends Biochem. Sci., 1989, 14, p 89–92

    Article  Google Scholar 

  34. Z.J. Sienkiewicz, N.A. Cridland, C.I. Kowalczuk, and R.D. Saunders, Biological Effects of Electromagnetic Fields and Radiation, The Review of Radio Science 1990–1992, M.R. Stone, Ed., Oxford Science Publications, Oxford, 1993, p 737–770

    Google Scholar 

  35. A. Kodama, N. Kamei, G. Kamei, W. Kongcharoensombat, S. Ohkawa, A. Nakabayashi, and M. Ochi, In Vivo Bioluminescence Imaging of Transplanted Bone Marrow Mesenchymal Stromal Cells Using a Magnetic Delivery System in a Rat Fracture Model, Br. J. Bone Joint Surg., 2012, 94, p 998–1006

    Article  Google Scholar 

  36. J.I. Jacobson, R. Gorman, W.S. Yamanashi, B.B. Saxena, and L. Clayton, Low-Amplitude, Extremely Low Frequency Magnetic Fields for the Treatment of Osteoarthritic Knees: A Double-Blind Clinical Study, Altern. Ther. Health Med., 2001, 7(5), p 54–64

    Google Scholar 

  37. R. Zboril, M. Mashlan, and D. Petridis, Iron(III) Oxides from Thermal Processes Synthesis, Structural and Magnetic Properties, Mössbauer Spectroscopy Characterization, and Applications, Chem. Mater., 2002, 14(3), p 969–982

    Article  Google Scholar 

  38. H.M. Kothari, E.A. Kulp, S.J. Limmer, P. Poizot, E.W. Bohannan, and J.A. Switzer, Electrochemical Deposition and Characterization of Fe3O4 Films Produced by the Reduction of Fe(III)-Triethanolamine, J. Mater. Res., 2006, 21(1), p 293–301

    Article  Google Scholar 

  39. M.E. Bahrololoom, M. Javidi, S. Javadpour, and J. Ma, Characterisation of Natural Hydroxyapatite Extracted from Bovine Cortical Bone Ash, J. Ceram. Process. Res., 2009, 10, p 129–138

    Google Scholar 

  40. K. Haberko, M.M. Bucko, J. Brzezińska-Miecznik, M. Haberko, W. Mozgawa, T. Panz, A. Pyda, and J. Zar, ebski, Natural Hydroxyapatite—Its Behaviour During Heat Treatment, J. Eur. Ceram. Soc., 2006, 26, p 537–542

    Article  Google Scholar 

  41. Y. Li, C.T. Nam, and C.P. Ooi, Iron (III) and Manganese (II) Substituted Hydroxyapatite Nanoparticles: Characterization and Cytotoxicity Analysis, J. Phys., 2009, 187(1), p 012024

    Google Scholar 

  42. R.P. Franke and F. Jung, Interaction of Blood Components and Blood Cells with Body Foreign, Surfaces, Ser. Biomech., 2012, 27, p 51–58

    Google Scholar 

  43. Genel Histoloji Erkocak, Dag Okan, Yay ltd. sti, Istanbul, 1983

    Google Scholar 

  44. R. Glicklis, L. Shapiro, R. Agbaria, J.C. Merchuk, and S. Cohen, Hepatocyte Behavior Within Three-Dimensional Porous Alginate Scaffolds, Biotechnol. Bioeng., 2000, 67, p 344–353

    Article  Google Scholar 

  45. E. McCafferty, Relationship Between the Isoelectric Point (pHpzc) and the Potential of Zero Charge (E pzc) for Passive Metals, Electrochim. Acta, 2010, 55, p 1630–1637

    Article  Google Scholar 

  46. M. Kosmulski, pH-Dependent Surface Charging and Points of Zero Charge, J. Colloid Interface Sci., 2006, 298, p 730–741

    Article  Google Scholar 

  47. M. Kosmulski, The pH-Dependent Surface Charging and Points of Zero Charge, J. Colloid Interface Sci., 2011, 353, p 1–15

    Article  Google Scholar 

  48. F. Bistolfi, Campi magnetici in medicina, Ed. Minerva Medica, Torino, 1993

    Google Scholar 

  49. C.W. Smith and S. Best, Electromagnetic Man, J.M. Dent & Sonns, London, 1989

    Google Scholar 

  50. F. Bistolfi, , Radiazioni non ionizzanti, ordine, disordine e biostruture, Ed. Minerva Medica, Torino, 1989

    Google Scholar 

  51. M. Cifra, J.Z. Fields, and A. Farhadi, Electromagnetic Cellular Interactions, Prog. Biophys. Mol. Biol., 2011, 105, p 223–246

    Article  Google Scholar 

  52. H. Fröhlich, The Extraordinary Dielectric Properties of Biological Materials and the Action of Enzymes, Proc. Natl. Acad. Sci., 1975, 72, p 4211–4215

    Article  Google Scholar 

  53. C. Rossi, A. Foletti, A. Magnani, and S. Lamponi, New Perspectives in Cell Communication: Bioelectromagnetic Interactions, Semin. Cancer Biol., 2011, 21, p 207–214

    Article  Google Scholar 

  54. S. Seckiner Gorgun, Studies on the Interaction Between Electromagnetic Fields and Living Matter Neoplastic Cellular Culture, Front. Prospect., 1998, 7(2), p 1–21

    Google Scholar 

  55. L.-Y. Sun, D.-K. Hsieh, Y. Tzai-Chiu, H.-T. Chiu, L. Sheng-Fen, G.-H. Luo, T.K. Kuo, O.K. Lee, and T.W. Chiou, Effect of Pulsed Electromagnetic Field on the Proliferation and Differentiation Potential of Human Bone Marrow Mesenchymal Stem Cells, Bioelectromagnetics, 2009, 30, p 251–260

    Article  Google Scholar 

  56. M.A. Omar, Elementary Solid State Physics, Pearson Education India, New Delhi, 1999

    Google Scholar 

  57. W. Adey, Biological Effects of Electromagnetic Fields, J. Cell. Biochem., 1993, 51, p 410–416

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. Maleki-Ghaleh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maleki-Ghaleh, H., Aghaie, E., Nadernezhad, A. et al. Influence of Fe3O4 Nanoparticles in Hydroxyapatite Scaffolds on Proliferation of Primary Human Fibroblast Cells. J. of Materi Eng and Perform 25, 2331–2339 (2016). https://doi.org/10.1007/s11665-016-2086-4

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11665-016-2086-4

Keywords

Navigation