Synthesis of nanostructured porous silica coatings on titanium and their cell adhesive and osteogenic differentiation properties
Débora Inzunza
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorCorresponding Author
Cristian Covarrubias
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Correspondence to: C. Covarrubias; e-mail: [email protected]Search for more papers by this authorAlfredo Von Marttens
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorYerko Leighton
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorJuan Carlos Carvajal
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorFrancisco Valenzuela
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorMario Díaz-Dosque
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorNicolás Méndez
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorConstanza Martínez
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorAna María Pino
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorJuan Pablo Rodríguez
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorMónica Cáceres
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorPatricio Smith
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorDébora Inzunza
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorCorresponding Author
Cristian Covarrubias
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Correspondence to: C. Covarrubias; e-mail: [email protected]Search for more papers by this authorAlfredo Von Marttens
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorYerko Leighton
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorJuan Carlos Carvajal
Departamento de Prótesis, Facultad de Odontología, Universidad de Chile, Chile
Search for more papers by this authorFrancisco Valenzuela
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorMario Díaz-Dosque
Departamento de Ciencias Básicas, Laboratorio de Nanobiomateriales, Facultad de Odontología, Universidad de Chile, Sergio Livingstone 943, Independencia, Santiago, Chile
Search for more papers by this authorNicolás Méndez
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorConstanza Martínez
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorAna María Pino
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorJuan Pablo Rodríguez
Laboratorio de Biología Celular, INTA, Universidad de Chile, Chile
Search for more papers by this authorMónica Cáceres
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorPatricio Smith
Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
Search for more papers by this authorAbstract
Nanostructured porous silica coatings were synthesized on titanium by the combined sol–gel and evaporation-induced self-assembly process. The silica-coating structures were characterized by X-ray diffraction, transmission electron microscopy, scanning electron microscopy, and nitrogen sorptometry. The effect of the nanoporous surface on apatite formation in simulated body fluid, protein adsorption, osteoblast cell adhesion behavior, and osteogenic differentiation of human bone marrow mesenchymal stem cells (hBMSCs) is reported. Silica coatings with highly ordered sub-10 nm porosity accelerate early osteoblast adhesive response, a favorable cell response that is attributed to an indirect effect due to the high protein adsorption observed on the large-specific surface area of the nanoporous coating but is also probably due to direct mechanical stimulus from the nanostructured topography. The nanoporous silica coatings, particularly those doped with calcium and phosphate, also promote the osteogenic differentiation of hBMSCs with spontaneous mineral nodule formation in basal conditions. The bioactive surface properties exhibited by the nanostructured porous silica coatings make these materials a promising alternative to improve the osseointegration properties of titanium dental implants and could have future impact on the nanoscale design of implant surfaces. © 2013 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 102A: 37–48, 2014.
REFERENCES
- 1Hedia HS, Mahmoud NA.Design optimization of functionally graded dental implant.Biomed Mater Eng2005; 14: 133–143.
- 2Davies JE.Understanding peri-implant endosseous healing.J Dent Educ2003; 67: 932–949.
- 3Marco F, Milena F, Gianluca G, Vittoria O.Periimplant osteogenesis in health and osteoporosis.Micron2005; 36: 630–644.
- 4Le Gue'hennec L, Soueidan A, Layrolle P, Amouriq Y.Surface treatments of titanium dental implants for rapid osseointegration.Dent Mater2007; 23: 844–854.
- 5Wennerberg A, Albrektsson T, Albrektsson B, Krol JJ.Histomorphometric and removal torque study of screw-shaped titanium implants with three different surface topographies.Clin Oral Implan Res1996; 6: 24–30.
- 6Wennerberg A, Hallgren C, Johansson C, Danelli SA.A histomorphometric evaluation of screw-shaped implants each prepared with two surface roughnesses.Clin Oral Implan Res1998; 9: 11–19.
- 7Cochran DL.A comparison of endosseous dental implant surfaces.J Periodontol1999; 70: 1523–1539.
- 8Shalabi MM., Gortemaker A, Van't Hof MA, Jansen JA, Creugers NHJ.Implant surface roughness and bone healing: A systematic review.J Dent Res2006; 85: 496–500.
- 9Mendonça G, Mendonca DBS, Arago FJL, Cooper LF.Advancing dental implant surface technology—From micron- to nanotopography.Biomaterials2008; 29: 3822–3835.
- 10Park J, Bauer S, Schlegel KA, Neukam FW, Mark KV, Schmuki P.TiO2 nanotube surfaces: 15 nm—An optimal length scale of surface topography for cell adhesion and differentiation.Small2009; 5: 666–671.
- 11McNamara LE, McMurray RJ, Biggs MJP, Kantawong F, Oreffo ROC, Dalby MJ.Nanotopographical control of stem cell differentiation.J Tissue Eng2010; 2010: 120623.
- 12Puckett S, Pareta R, Webster TJ.Nano rough micron patterned titanium for directing osteoblast morphology and adhesion.Int J Nanomed2008; 3: 229–241.
- 13Oliveira PT, Nanci A.Nanotexturing of titanium-based surfaces upregulates expression of bone sialoprotein and osteopontin by cultured osteogenic cells.Biomaterials2004; 25: 403–413.
- 14Subramanian K, Tran D, Nguyen KT. Cellular responses to nanoscale surface modifications of titanium implants for dentistry and bone tissue engineering applications. In: K Subramani, W Ahmed, editors. Emerging Nanotechnologies in Dentistry: Materials, Processes, and Applications.Oxford, UK:Elsevier;2012. p 115–117.
- 15Webster TJ, Ejiofor JU.Increased osteoblast adhesion on nanophase metals: Ti, Ti6Al4V, and CoCrMo.Biomaterials2004; 25: 4731–4739.
- 16Cooper LF, Zhou Y, Takebe J, Guo J, Abron A, Holmen A, Ellingsen JE.Fluoride modification effects on osteoblast behavior and bone formation at TiO2 grit-blasted c.p. titanium endosseous implants.Biomaterials2006; 27: 926–936.
- 17Ellingsen JE, Thomsen P, Lyngstadaas SP.Advances in dental implant materials and tissue regeneration.Periodontol 20002006; 41: 136–156.
- 18Domanski M, Luttge R, Lamers E, Walboomers XF, Winnubst L, Jansen JA, Gardeniers JGE,Submicron-patterning of bulk titanium by nanoimprint lithography and reactive ion etching,Nanotechnology2012; 23: 065306.
- 19Sul YT, Johansson C, Wennerberg A, Cho LR, Chang BS, Albrektsson T.Optimum surface properties of oxidized implants for reinforcement of osseointegration: Surface chemistry, oxide thickness, porosity, roughness, and crystal structure.Int J Oral Maxillofac Implants2005; 20: 349–359.
- 20Lee SH, Kim HW, Lee EJ, Li LH, Kim HE.Hydroxyapatite–TiO2 hybrid coating on Ti implants.J Biomater Appl2006; 20: 195–208.
- 21Germanier Y, Tosatti S, Broggini N, Textor M, Buser D.Enhanced bone apposition around biofunctionalized sandblasted and acid-etched titanium implant surfaces. A histomorphometric study in miniature pigs.Clin Oral Implants Res2006; 17: 251–257.
- 22Soler-Illia, GJAA, Sanchez C, Lebeau B, Patarin J.Designed hybrid organic–inorganic nanocomposites from functional nanobuilding blocks.Chem. Rev2001; 13: 3061–3083.
- 23Ariga K, Hill JP, Lee MV, Vinu A, Charvet R, Acharya S.Challenges and breakthroughs in recent research on self-assembly.Sci Technol Adv Mater2008; 9: 014109.
- 24Lu Y, Gangull R, Drewlen CA, Anderson MT, Brinker CJ, Gong W, Guo Y, Soyez H, Dunn B, Huang MH, Zink JI.Continuous formation of supported cubic and hexagonal mesoporous films by sol–gel dip-coating.Nature1997; 389: 364–368.
- 25Brinker CJ, Lu Y, Sellinger A, Fan H.Evaporation-induced self-assembly: nanostructures made easy.Adv Mater1999; 11: 579–585.
- 26Kuemmel M, Allouche J, Nicole L, Boissièe C, Laberty C, Amenitsch H, Sanchez C, Grosso D.A chemical solution deposition route to nanopatterned inorganic material surfaces.Chem Mater2007; 19: 3717–3725.
- 27Gomez-Vega JM, Hozumi A, Sugimura H, Takai O.Ordered mesoporous silica coatings that induce apatite formation in vitro.Adv Mater2001; 13: 822–825.
- 28Biggs MJP, Richards RG, Gadegaard, Wilkinson CDW, Dalby MJ.The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading.J Mater Sci: Mater Med2007; 18: 399–404.
- 29Cavalcanti-Adam EA, Volberg T, Micoulet A, Kessler H, Geiger B, Spatz JP.Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands.Biophys J2007; 92: 2964–2974.
- 30Dalby MJ, Riehle MO, Johnstone HJH, Affrossman S, Curtis ASG.Nonadhesive nanotopography: Fibroblast response to poly(n-butyl methacrylate)-poly(styrene) demixed surface features.J Biomed Mater Res A2003; 67: 1025–1032.
- 31Cavalcanti-Adam EA, Micoulet A, Bummel J, Auernheimer J, Kessler H, Spatz JP.Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly.Eur J Cell Biol2006; 85: 219–224.
- 32Dalby MJ, Giannaras D, Riehle MO, Gadegaard N, Affrossman S, Curtis ASG.Rapid fibroblast adhesion to 27 nm high polymer demixed nano-topography.Biomaterials2004; 25: 77–83.
- 33Sjstrom T, Dalby MJ, Hart A, Tare R, Oreffo ROC, Su B.Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells.Acta Biomater2009; 5: 1433–1441.
- 34Izquierdo-Barba I, Arcos D, Sakamoto Y, Terasaki O, López-Noriega A, Vallet-Regí M.High performance mesoporous bioceramics mimicking bone mineralization.Chem Mater2008; 20: 3191–3198.
- 35Mabande GTP, Ghosh S, Lai Z, Schwieger W, Tsapatsis M.Preparation of b-oriented MFI films on porous stainless steel substrates.Ind Eng Chem Res2005; 44: 9086–9095.
- 36Kokubo T, Kushitani H, Sakka S, Kitsugi T, Yamamuro T.Solution able to reproduce in vivo surface-structure change in bioactive glass–ceramic A-W.J Biomed Mater Res1990; 24: 723–734.
- 37Alberius PCA, Frindell KL, Hayward RC, Kramer WJ, Stucky GD, Chmelka BF.General predictive syntheses of cubic, hexagonal, and lamellar silica and titania mesostructured thin films.Chem Mater2002; 14: 3284–3294.
- 38Yamada T., Zhou H-S, Uchida H, Tomita M, Ueno Y, Ichino T, Honma I, Asai K. Katsube T.Photovoltage no gas sensor with properties dependent on the structure of the self-ordered mesoporous silicate film.Adv Mater2002; 14: 812–815.
- 39Miyaji F, Iwai M, Kokubo T, Nakamura T.Effect of heat treatment on apatite-forming ability of Ti metal induced by alkali treatment.J Mater Sci: Mater Med1998; 9: 61–65.
- 40López-Noriega A, Arcos D, Izquierdo-Barba I, Sakamoto Y, Terasaki, O, M. Vallet-Regí.Ordered mesoporous bioactive glasses for bone tissue regeneration.Chem Mater2006; 18: 3137–3144.
- 41Kokubo T, Takadama H.How useful is SBF in predicting in vivo bone bioactivity.Biomaterials2006; 27: 2907–2915.
- 42Rajaraman R, Rounds DE, Yen SPS, Rembaum A.A scanning electron microscope study of cell adhesion and spreading in vitro.Exp Cell Res1974; 88: 327–339.
- 43Balto H, Al-Nazhan S.Attachment of human periodontal ligament fibroblasts to three different root-end filling materials. Scanning electron microscope observation.Oral Surg2003; 95: 222–227.
- 44Anselme K.Osteoblast adhesion on biomaterials.Biomaterials2000; 21: 667–681.
- 45Hirayama K, Akashi S, Furuya M, Fukuhara K.Rapid confirmation and revision of the primary structure of bovine serum albumin by ESIMS and Frit-FAB LC/MS.Biochem Biophys Res Commun1990; 173: 639–646.
- 46Cacciafesta P, Humphries ADL, Jandt KD, Miles MJ.Human plasma fibrinogen adsorption on ultraflat titanium oxide surfaces studied with atomic force microscopy.Langmuir2000; 16: 8167–8175.
- 47Covarrubias C, Quijada R.High catalytic activity of SBA-15-supported metallocene toward ethylene polymerization: The effect of the ordered porous structure of the support.Catal Commun2009; 10: 995–1001.
- 48Nishimura T, Takeichi M.Remodeling of the adherens junctions during morphogenesis.Curr Top Dev Biol2009; 89: 33–54.
- 49Boonrungsimana S, Gentlemana E, Carzanigad R, Evansa ND, McComba DW, Portera AE, Stevensa MM.The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation.PNAS2012; 109: 14170–14175.
- 50Anderson HC.Matrix vesicles and calcification.Curr Rheumatol Rep2003; 5: 222–226.
- 51Declercq H, Van den Vreken H, De Maeyer D, Verbeeck R, Schacht E, De Ridder L, Cornelissen M.Isolation, proliferation and differentiation of osteoblastic cells to study cell/biomaterial interactions: Comparison of different isolation techniques and source.Biomaterials2004; 25: 757–768.
- 52Guo J, Padilla RJ, Ambrose W, De Kok IJ, Cooper LF.Modification of TiO2 grit blasted titanium implants by hydrofluoric acid treatment alters adherent osteoblast gene expression in vitro and in vivo.Biomaterials2007; 28: 5418–5425.
- 53Iza ZM, Schneider GB, Zaharias R, Seabold D. Stanford CM.Effects of fluoride-modified titanium surfaces on osteoblast proliferation and gene expression.Int J Oral Maxillofac Implants2006; 2: 203–211.
- 54Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS.Control of stem cell fate by physical interactions with the extracellular matrix.Cell Stem Cell2009; 5( 1): 17–26.
- 55Kulangara K, Yang Y, Yang J, Leong KW.Nanotopography as modulator of human mesenchymal stem cell function.Biomaterials2012; 33: 4998–5003.
- 56Tsigkou O, Jones JR, Polak JM, Stevens MM.Differentiation of fetal osteoblasts and formation of mineralized bone nodules by 45S5 Bioglass conditioned medium in the absence of osteogenic supplements.Biomaterials2009; 21: 3542–3550.
- 57Bielby RC, Christodoulou IS, Pryce RS, Radford WJ, Hench LL, Polak JM.Time- and concentration-dependent effects of dissolution products of 58S sol–gel bioactive glass on proliferation and differentiation of murine and human osteoblasts.Tissue Eng2004; 10: 1018–1026.