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Osteogenic differentiation of bone marrow-derived mesenchymal stem cells on anodized niobium surface

  • Tissue Engineering Constructs and Cell Substrates
  • Original Research
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Abstract

Currently, titanium and its alloys are the most used materials for biomedical applications. However, because of the high costs of these metals, new materials, such as niobium, have been researched. Niobium appears as a promising material due to its biocompatibility, and excellent corrosion resistance. In this work, anodized niobium samples were produced and characterized. Their capacity to support the osteogenic differentiation of bone marrow-derived mesenchymal stem cells (BM-MSCs) was also tested. The anodized niobium samples were characterized by SEM, profilometry, XPS, and wettability. BM-MSCs were cultured on the samples during 14 days, and tested for cell adhesion, metabolic activity, alkaline phosphatase activity, and mineralization. Results demonstrated that anodization promotes the formation of a hydrophilic nanoporous oxide layer on the Nb surface, which can contribute to the increase in the metabolic activity, and in osteogenic differentiation of BM-MSCs, as well as to the extracellular matrix mineralization.

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References

  1. Grow (2016) Critical raw materials. http://ec.europa.eu/growth/sectors/raw-materials/specific-interest/critical_pt. Accessed October 2016.

  2. Findlay DM, Welldon K, Atkins GJ, Howie DW, Zannettino ACW, Bobyn D. The proliferation and phenotypic expression of human osteoblasts on tantalum metal. Biomaterials. 2004;25:2215–27.

    Article  CAS  Google Scholar 

  3. Bobyn JD, Toth KK, Hacking SA, Tanzer M, Krygier JJ. Tissue response to porous tantalum acetabular cups: a canine model. J Arthoplasty. 1999;14:347–54.

    Article  CAS  Google Scholar 

  4. Wang X, Li Y, Xiong J, Hodgson PD, Wen C. Porous TiNbZr alloy scaffolds for biomedical applications. Acta Biomaterialia. 2009;5:3616–24.

    Article  CAS  Google Scholar 

  5. Metikoš-Huković M, Kwokal A, Piljac J. The influence of niobium and vanadium on passivity of titanium-based implants in physiological solution. Biomaterials. 2003;24:3765–75.

    Article  Google Scholar 

  6. Alves AR, Coutinho AR. The evolution of the niobium production in Brazil. Mater Res. 2015;18:106–12.

    Article  Google Scholar 

  7. Nasser SN, Guo WG, Cheng JY. Mechanical properties and deformation mechanisms of a commercially pure titanium. Acta Materialia. 1999;47:3705–20.

    Article  Google Scholar 

  8. Eisenbarth E, Velten D, Müller M, Thull R, Brene J. Biocompatibility of β-stabilizing elements of titanium alloys. Biomaterials. 2004;25:5705–13.

    Article  CAS  Google Scholar 

  9. Olivares-Navarrete R, Olaya JJ, Ramírez C, Rodil SE. Biocompatibility of niobium coatings. Coatings. 2011;1:72–87.

    Article  CAS  Google Scholar 

  10. Kokubo T. Apatite formation on surfaces of ceramics, metals and polymers in body environment. Acta Materialia. 1998;46:2519–27.

    Article  CAS  Google Scholar 

  11. Fernandes GVO, Alves GG, Linhares ABR, Da Silva MHO, Granjeiro JM. Evaluation of cytocompatibility of bioglass-niobium granules with human primary osteoblasts: a multiparametric approach. Key Eng Mater. 2012;493-494:37–42.

    Article  CAS  Google Scholar 

  12. Gittens RA, Scheideler L, Rupp F, Hyzy SL, Gerstorfer JG, Schwartz Z, et al. A review on the wettability of dental implant surfaces II: biological and clinical aspects. Acta Biomaterialia. 2014;10:2907–18.

    Article  CAS  Google Scholar 

  13. Spriano S, Chandra VS, Cochis A, Uberti F, Rimondini L, Bertone E, et al. How do wettability, zeta potential and hydroxylation degree affect the biological response of biomaterials? Mater Sci Eng C. 2017;74:542–55.

    Article  CAS  Google Scholar 

  14. Peng-Yuan W, Wen-Tyng L, Jiashing Y, Wei-Bor T. Modulation of osteogenic, adipogenic and myogenic differentiation of mesenchymal stem cells by submicron grooved topography. J Mater Sci: Mater Med. 2012;23:3015–28.

    Google Scholar 

  15. Xie Y, Zheng X, Huang L, Ding C. Influence of hierarchical hybrid micro/nano-structured surface on biological performance of titanium coating. J Mater Sci. 2012;47:1411–7.

    Article  CAS  Google Scholar 

  16. Qin L, Zeng Q, Wang W, Zhang Y, Dong G. Response of MC3T3-E1 osteoblast cells to the microenvironment produced on Co-Cr-Mo alloy using laser surface texturing. J Mater Sci. 2014;49:2662–71.

    Article  CAS  Google Scholar 

  17. Bianchin ACV, Maldaner GR, Fuhr LT, Beltrami LVR, Malfatti CF, Rieder ES, et al. A model for the formation of niobium sctructures by anodization. Mater Res. 2017;20:1010–23.

    Article  CAS  Google Scholar 

  18. Sowa M, Kazek-Kesik A, Krzakala A, Socha RP, Dercz G. Modification of niobium surfaces using plasma electrolyte oxidation in silicate solutions. J Solid State Electrochem. 2014;18:3129–42.

    Article  CAS  Google Scholar 

  19. Huang HH, Wu CP, Sun YS, Yang WE, Lee TH. Surface nanotopography of an anodized Ti-6Al6-7Nb alloy enhances cell growth. J Alloy Compd. 2014;615:s648–54.

    Article  CAS  Google Scholar 

  20. Gao Y, Gao B, Wang R, Wu J, Zhang LJ, Hao YL, et al. Improved biological performance of low modulus Ti-24Nb-4Zr-7,9Sn implants due to surface modification by anodic oxidation. Appl Surf Sci. 2009;255:5009–15.

    Article  CAS  Google Scholar 

  21. Rani RA, Zoolfakar AS, Zhen J, Kadir RAB, Nili H, Latham K, et al. Reduced impurity-driven defect states in anodized nanoporous Nb2O5: the possibility of improving performance of photoanodes. Chem Commun. 2013;49:6349–51.

    Article  CAS  Google Scholar 

  22. Galstyan V, Comini E, Faglia G, Sberveglieri G. Synthesis of self-ordered and well-aligned Nb2O5 nanotubes. CrystEngComm. 2014;16:10273–9.

    Article  CAS  Google Scholar 

  23. Pidwirny M (2006) Atmospheric Composition, Fundamentals of Physical Geography 2nd edn.

  24. Park KH, Kang JW, Lee EM, Kim JS, Rhee YH, Kim M, et al. Melatonin promotes osteoblastic differentiation through the BMP/ERK/Wnt signaling pathways. J Pineal Res. 2011;51:187–94.

    Article  CAS  Google Scholar 

  25. Zhou X, Li Z, Wang Y, Sheng X, Zhang Z. Photoluminescence of amorphous niobium oxide films synthesized by solid-state reaction. Thin Solid Films. 2008;516:4213–6.

    Article  CAS  Google Scholar 

  26. Pereira BL, Lepienski CM, Mazzaro I, Kuromoto NK. Apatite grown in niobium by two-step plasma electrolytic oxidation. Mater Sci Eng C. 2017;77:1235–41.

    Article  CAS  Google Scholar 

  27. Farha AH, Ozkendir OM, Elsayed-Ali HE, Myneni G, Ufuktepe Y. The effect of heat treatment on structural and electronic properties of niobium nitride prepared by a thermal diffusion method. Surf Coat Technol. 2017;309:54–8.

    Article  CAS  Google Scholar 

  28. Oikawa Y, Minami T, Mayama H, Tsujii M, Fushimi K, Aoki Y, et al. Preparation of self-organized porous anodic niobium oxide microcones and their surface wettability. Acta Materialia. 2009;57:3941–6.

    Article  CAS  Google Scholar 

  29. Lim JH, Park G, Choi J. Synthesis of niobium oxide nanopowders by field-crystallization-assisted anodization. Curr Appl Phys. 2012;12:155–9.

    Article  Google Scholar 

  30. Miller DJ, Biesinger MC, Mcintyre NS. Interactions of CO2 and CO at fractional atmosphere pressures with iron and iron oxide surfaces: one possible mechanism for surface contamination? Surf Interface Anal. 2002;33:299–305.

    Article  CAS  Google Scholar 

  31. Beamson G, Briggs D (1992) High resolution XPS of organic polymers, The Scienta ESCA300 Database Wiley Interscience. New York, NY.

  32. Rouxhet PG, Genet MJ. XPS analysis of bio-organic systems. Surf Interface Anal. 2012;43:1453–70.

    Article  Google Scholar 

  33. Ozer N, Rubin MD, Lampert CM. Optical and electrochemical characteristics of niobium oxide films prepared by sol–gel process and magnetron sputtering A comparison. Sol Energy Mater Sol Cells. 1996;40:285–96.

    Article  Google Scholar 

  34. Lucci M, Thann HN, Davoli I. Electron spectroscopy analysis on NbN to grow and characterize NbN/AlN/NbN Josephson junction. Superlattices Microstructures. 2008;43:518–23.

    Article  CAS  Google Scholar 

  35. Hryniewicz T, Rokosz K, Zschommler Sandim HR. SEM/EDX and XPS studies of niobium after electropolishing. Appl Surf Sci. 2012;263:357–61.

    Article  CAS  Google Scholar 

  36. Kubacki J, Molak A, Talik E. Eletronic structure of NaNbO3—Mn single crystals. J Alloy Compd. 2001;328:156–61.

    Article  CAS  Google Scholar 

  37. Stojadinovic S, Vasilic R. Orange-red photoluminescence of Nb2O5:Eu3+, Sm3+ coatings formed by plasma electrolytic oxidation of niobium. J Alloy Compd. 2016;685:881–9.

    Article  CAS  Google Scholar 

  38. Cottineau T, Béalu N, Gross PA, Pronkin SN, Keller N, Savinova ER, et al. One step synthesis of niobium doped titania nanotube arrays to form (N,Nb) co-doped TiO2 with high visible light photoelectrochemical activity. J Mater Chem A. 2013;1:2151–60.

    Article  CAS  Google Scholar 

  39. Marques MT, Ferraria AM, Correia JB, Botelho do Rego AM, Vilar R. XRD, XPS and SEM characterization of Cu-NbC nanocomposite produced by mechanical alloying. Mater Chem Phys. 2008;109:174–80.

    Article  CAS  Google Scholar 

  40. Jung K, Kim Y, Park YS, Jung W, Choi J, Park B, et al. Unipolar resistive switching in insulating niobium oxide film and probing electroforming induced metallic components. J Appl Phys. 2011;109:054511-1–4.

    Google Scholar 

  41. Tian H, Reece CE, Kelly MJ, Wang S, Plucinski L, Smith KE, et al. Surface studies of niobium chemically polished under conditions for superconducting radio frequency (SRF) cavity production. Appl Surf Sci. 2006;253:1236–42.

    Article  CAS  Google Scholar 

  42. Sreekantan S, Saharudin KA, Wei LC. Formation of TiO2 nanotubes via anodization and potential applications for photocatalysts, biomedical materials, and photoelectrochemical cell. IOP Conf Ser: Mater Sci Eng. 2011;21:1–19.

    Article  Google Scholar 

  43. Escada AL, Nakazato RZ, Claro APR. Influence of anodization parameters in the TiO2 nanotubes formation on Ti-7.5Mo alloy surface for biomedical application. Mater Res. 2017;20:1282–90.

    Article  CAS  Google Scholar 

  44. Stepniowski WJ, Moneta M, Norek M, Domanska MM, Scarpellini A, Scalerno M. The influence of electrolyte composition on the growth of nanoporous anodic alumina. Electrochim Acta. 2016;211:453–60.

    Article  CAS  Google Scholar 

  45. Elias CN, Oshida Y, Lima JHC, Muller CA. Relationship between surface properties (roughness, wettability and morphology) of titanium and dental implant removal torque. J Mech Behav Biomed Mater. 2008;1:234–42.

    Article  Google Scholar 

  46. Tran PA, Webster TJ. Understanding the wetting properties of nanostructured selenium coatings: the role of nanostructured surface roughness and air-pocket formation. Int J Nanomed. 2013;8:2001–9.

    Google Scholar 

  47. Kubiak KJ, Wilson MCT, Mathia TG, Carval Ph. Wettability versus roughness of engineering surfaces. Wear. 2011;271:523–8.

    Article  CAS  Google Scholar 

  48. Sharma A, McQuillan AJ, Sharma LA, Waddell JN, Shibata Y, Duncan WJ. Spark anodization of titanium-zirconium alloy: surface characterization and bioactivity assessment. J Mater Sci: Mater Med. 2015;26:1–11.

    Google Scholar 

  49. Wu E-Y, Ou K-L, Ou S-F, Jandt KD, Pan Y-N. Effect of O2-plasma treatment on surface characteristics and osteoblast-like MG-63 cells response of Ti-30Nb-1Fe-1Hf alloy. Mater Trans. 2009;50:891–8.

    Article  CAS  Google Scholar 

  50. Kesik AK, Lesniak K, Orzechowska BU, Drab M, Wisniewska A, Simka W. Alkali treatment of anodized titanium alloys affects cytocompatibility. Metals. 2018;8:1–11.

    Google Scholar 

  51. Kanuru RK, Sugita Y, Ikeda T, Shinwari H, Ishijima M, Honda Y, et al. Titanium delivery of osteoblastic cell sheets: an in vitro study. J Hard Tissue Biol. 2018;27:43–50.

    Article  CAS  Google Scholar 

  52. Wang T, Wan Y, Liu Z. Fabrication of hierarchical micro/nanotopography on bio-titanium alloy surface for cytocompatibility improvement. J Mater Sci. 2016;51:9551–61.

    Article  CAS  Google Scholar 

  53. Xu J, Weng X-J, Wang X, Huang J-Z, Zhang C, Muhammad H, et al. Potential use of porous titanium-niobium alloy in orthopedic implants: preparation and experimental study of its biocompatibility in vitro. PLoS One. 2013;8:e79289–e79289.

    Article  Google Scholar 

  54. Li Y, Yang C, Zhao H, Qu S, Li X, Li Y. New developments of Ti-based alloys for biomedical applications. Materials. 2014;7:1709–800.

    Article  Google Scholar 

  55. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26:5474–91.

    Article  CAS  Google Scholar 

  56. Patel S, Butt A, Tao Q, Royhman D, Sukotjo C, Takoudis CG. Novel functionalization of Ti-V alloy and Ti-II using atomic layer deposition for improved surface wettability. Colloids Surf B: Biointerfaces. 2014;115:280–5.

    Article  CAS  Google Scholar 

  57. Boukari A, Francius G, Hemmerlé J. AFM force spectroscopy of the fibrinogen adsorption process onto dental implants. J Biomed Mater Res Part A. 2006;78:466–72.

    Article  Google Scholar 

  58. Bacchelli B, Giavaresi G, Franchi M. Influence of a zirconia sandblasting treated surface on peri-implant bone healing: an experimental study in sheep. Acta Biomaterialia. 2009;5:2246–57.

    Article  CAS  Google Scholar 

  59. Guehennec Laurent L, Lopez-Heredia MA, Enkel B, Weiss P, Amouriq Y, Layrolle P. Osteoblastic cell behaviour on different titanium implant surfaces. Acta Biomaterialia. 2008;4:535–43.

    Article  Google Scholar 

  60. Rausch-fan X, Zhe Q, Marco W, Michael M, Andreas S. Differentiation and cytokine synthesis of human alveolar osteoblasts compared to osteoblast-like cells (MG63) in response to titanium surfaces. Dent Mater. 2008;24:102–10.

    Article  CAS  Google Scholar 

  61. Mackey AC, Karlinsey RL, Chu T-MG, MacPherson M, Alge DL. Development of niobium oxide coatings on sand-blasted titanium alloy dental implants. Mater Sci Appl. 2012;3:301–5.

    CAS  Google Scholar 

  62. Mestieri LB, Gomes-Cronélio AL, Rodrigues EM, Faria G, Guerreiro-Tanomaru JM, Tanomaru-Filho M. Cytotoxicity and bioactivity of calcium silicate cements combined with niobium oxide in different cell lines. Braz Dent J. 2017;28:65–71.

    Article  Google Scholar 

  63. Mestieri LB, Tanomaru-Filho M, Gomes-Cornélio AL, Salles LP, Bernardi MIB, Guerreiro-Tanomaru JM. Radiopacity and cytotoxicity of Portland cement associated with niobium oxide micro and nanoparticles. J Appl Oral Sci. 2014;22:554–9.

    Article  Google Scholar 

  64. Young MD, Tran N, Tran PA, Jarrel JD, Hayda RA, Born CT. Niobium oxide–polydimethylsiloxane hybrid composite coatings fortuning primary fibroblast functions. J Biomed Mater Res A. 2014;102A:1478–85.

    Article  CAS  Google Scholar 

  65. Velten D, Eisenbarth E, Schanne N, Breme J. Biocompatible Nb2O5 thin films prepared by means of the sol-gel process. J Mater Sci: Mater Med. 2004;15:457–61.

    CAS  Google Scholar 

  66. Eisenbarth E, Velten D, Muller M, Thull R, Breme J. Nanostructured niobium oxide coatings influence osteoblast adhesion. J Biomed Mater Res Part A. 2006;79:166–75.

    Article  CAS  Google Scholar 

  67. Denry I, Holloway J, Nakkula R, Walters J. Effect of niobium content on the microstructure and thermal properties of fluorapatite glass-ceramics. J Biomed Mater Res Part B: Appl Biomater. 2005;75:18–24.

    Article  CAS  Google Scholar 

  68. Kushwaha M, Pan X, Holloway JA, Denry IL. Differentiation of human mesenchymal stem cells on niobium-doped fluorapatite glass-ceramics. Dent Mater. 2012;28:252–60.

    Article  CAS  Google Scholar 

  69. Medda R, Helth A, Herre P, Pohl D, Rellinghaus B, Perschmann N, et al. Investigation of early cell–surface interactions of human mesenchymal stem cells on nanopatterned β-type titanium–niobium alloy surfaces. Interface Focus. 2014;4:1–10.

    Article  Google Scholar 

  70. Vandrovcova M, Jirka I, Novotna K, Lisa V, Frank O, Kolska Z, et al. Interaction of human osteoblast-like Saos-2 and MG-63 cells with thermally oxidized surfaces of a titanium-niobium alloy. PLOS one. 2014;9:e100475.

    Article  Google Scholar 

  71. Dacca A, Gemme G, Mattera L, Parodi R. XPS analysis of the surface composition of niobium for superconducting RF cavities. Appl Surf Sci. 1998;126:219–30.

    Article  CAS  Google Scholar 

  72. Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracelular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001;2:793–805.

    Article  CAS  Google Scholar 

  73. Khalil AS, Xie AW, Purphy WL. Context clues: the importance of stem cell-material interactions. ACS Chem Biol. 2014;9:45–56.

    Article  CAS  Google Scholar 

  74. Tamura Y, Takeuchi Y, Suzawa M, Fukumoto S, Kato M, Miyazono K, et al. Focal adhesion kinase activity is required for bone morphogenetic protein – smad1 signaling and osteoblastic differentiation in murine MC3T3-E1 cells. J Bone Miner Res. 2001;16:1772–9.

    Article  CAS  Google Scholar 

  75. Kasemo B. Biological surface science. Surf Sci. 2002;500:656–77.

    Article  CAS  Google Scholar 

  76. Latour Jr. RA, Wnek GE, Bowlin GL (2014) Encyclopedia of biomaterials and biomedical engineering, second edition, Cleveland, USA.

  77. Johansson CB, Albrektsson T. A removal torque and histomorphometric study of commercially pure niobium and titanium implants in rabbit bone. Clin Oral Implants Res. 1991;2:24–9.

    Article  CAS  Google Scholar 

  78. Matsuno H, Yokoyama A, Watari F, Uo M, Kawasaki T. Biocompatibility and osteogenesis of refractory metal implants, titanium, hafnium, niobium, tantalum and rhenium. Biomaterials. 2001;22:1253–62.

    Article  CAS  Google Scholar 

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Acknowledgements

The present work was carried out with the support of CAPES (Brazilian Coordination for the Improvement of Higher Education Personnel), and CNPq (National Council for Scientific and Technological Development). The authors would like to thank Valeria Pinhatti (from Universidade Luterana do Brasil—ULBRA, Brazil), for her technical services related to cell culture.

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Authors and Affiliations

  1. LAPEC/PPGE3M, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Prédio 43427, Sala 232, Porto Alegre, RS, 91501-970, Brazil

    Leonardo Marasca Antonini, Tiago Lemos Menezes, Adilar Gonçalves dos Santos Jr & Célia de Fraga Malfatti

  2. ELETROCORR/PPGE3M, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Prédio 43427, Sala 216, Porto Alegre, RS, 91501-970, Brazil

    Antonio Shigueaki Takimi

  3. FEEVALE, Universidade Feevale, Novo Hamburgo, RS, Brazil

    Denis Jardim Villarinho

  4. Laboratory of Tissue Engineering – BioTis, Inserm U1026, University of Bordeaux, 146 Rue Léo Saignat, Bât. 4A, 2ème étage, Bordeaux, 33076, France

    Bruno Paiva dos Santos

  5. Programa de Pós-graduação em Biologia Celular e Molecular Aplicada à Saúde (PPGBioSaúde), Universidade Luterana do Brasil, Laboratório de Células-Tronco e Engenharia de Tecidos, Av. Farroupilha, São José, Canoas, RS, 92425900, Brazil

    Melissa Camassola

  6. INPE, Instituto Nacional de Pesquisas Espaciais, Av. dos Astronautas, 1.758 - Jardim da Granja, São José dos Campos, SP, 12228-970, Brazil

    Jossano Saldanha Marcuzzo

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  1. Leonardo Marasca Antonini
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  2. Tiago Lemos Menezes
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Antonini, L.M., Menezes, T.L., dos Santos, A.G. et al. Osteogenic differentiation of bone marrow-derived mesenchymal stem cells on anodized niobium surface. J Mater Sci: Mater Med 30, 104 (2019). https://doi.org/10.1007/s10856-019-6305-z

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