Biofunctionalization of a titanium surface with a nano-sawtooth structure regulates the behavior of rat bone marrow mesenchymal stem cells

Background: The topography of an implant surface can serve as a powerful signaling cue for attached cells and can enhance the quality of osseointegration. A series of improved implant surfaces functionalized with nanoscale structures have been fabricated using various methods. Methods: In this study, using an H2O2 process, we fabricated two size-controllable sawtooth-like nanostructures with different dimensions on a titanium surface. The effects of the two nano-sawtooth structures on rat bone marrow mesenchymal stem cells (BMMSCs) were evaluated without the addition of osteoinductive chemical factors. Results: These new surface modifications did not adversely affect cell viability, and rat BMMSCs demonstrated a greater increase in proliferation ability on the surfaces of the nano-sawtooth structures than on a control plate. Furthermore, upregulated expression of osteogenic-related genes and proteins indicated that the nano-sawtooth structures promote osteoblastic differentiation of rat BMMSCs. Importantly, the large nano-sawtooth structure resulted in the greatest cell responses, including increased adhesion, proliferation, and differentiation. Conclusion: The enhanced adhesion, proliferation, and osteogenic differentiation abilities of rat BMMSCs on the nano-sawtooth structures suggest the potential to induce improvements in bone-titanium integration in vivo. Our study reveals the key role played by the nano-sawtooth structures on a titanium surface for the fate of rat BMMSCs and provides insights into the study of stem cell-nanostructure relationships and the related design of improved biomedical implant surfaces.

[1]  Lingzhou Zhao,et al.  The influence of hierarchical hybrid micro/nano-textured titanium surface with titania nanotubes on osteoblast functions. , 2010, Biomaterials.

[2]  K. Kendall,et al.  Surface energy and the contact of elastic solids , 1971, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

[3]  Patrik Schmuki,et al.  Nanosize and vitality: TiO2 nanotube diameter directs cell fate. , 2007, Nano letters.

[4]  M. Khorasani,et al.  Effect of oxygen plasma treatment on surface charge and wettability of PVC blood bag—In vitro assay , 2007 .

[5]  Q. Wang,et al.  The promotion of osteoblastic differentiation of rat bone marrow stromal cells by a polyvalent plant mosaic virus. , 2008, Biomaterials.

[6]  J. Nebe,et al.  The influence of surface roughness of titanium on beta1- and beta3-integrin adhesion and the organization of fibronectin in human osteoblastic cells. , 2005, Biomaterials.

[7]  Lyndon F Cooper,et al.  Advancing dental implant surface technology--from micron- to nanotopography. , 2008, Biomaterials.

[8]  Xuefeng Gao,et al.  Biophysics: Water-repellent legs of water striders , 2004, Nature.

[9]  Paul K. Chu,et al.  Surface nano-functionalization of biomaterials , 2010 .

[10]  D. Kaplan,et al.  Mandibular repair in rats with premineralized silk scaffolds and BMP-2-modified bMSCs. , 2009, Biomaterials.

[11]  P. Layrolle,et al.  Adhesion and osteogenic differentiation of human mesenchymal stem cells on titanium nanopores. , 2011, European cells & materials.

[12]  L F Cooper,et al.  Biologic determinants of bone formation for osseointegration: clues for future clinical improvements. , 1998, The Journal of prosthetic dentistry.

[13]  A. Curtis,et al.  The influence of microscale topography on fibroblast attachment and motility. , 2004, Biomaterials.

[14]  Steven S. Lapham,et al.  Thin Films , 1996, Science.

[15]  Sungho Jin,et al.  Stem cell fate dictated solely by altered nanotube dimension , 2009, Proceedings of the National Academy of Sciences.

[16]  Q. Wang,et al.  The synergistic effects of multivalent ligand display and nanotopography on osteogenic differentiation of rat bone marrow stem cells. , 2010, Biomaterials.

[17]  M. McKee,et al.  Chemical modification of titanium surfaces for covalent attachment of biological molecules. , 1998, Journal of biomedical materials research.

[18]  F. Fairbrother,et al.  CCCXII.—Studies in electro-endosmosis. Part I , 1924 .

[19]  A Curtis,et al.  Nantotechniques and approaches in biotechnology. , 2001, Trends in biotechnology.

[20]  A Curtis,et al.  Guidance and activation of murine macrophages by nanometric scale topography. , 1996, Experimental cell research.

[21]  N. Nakabayashi,et al.  The effect of phosphoric acid concentration on resin tag length and bond strength of a photo-cured resin to acid-etched enamel. , 2000, Dental materials : official publication of the Academy of Dental Materials.

[22]  P. Charbord,et al.  Culture and characterization of human bone marrow mesenchymal stem cells. , 2007, Methods in molecular medicine.

[23]  P. Krebsbach,et al.  Osterix Enhances BMSC-associated Osseointegration of Implants , 2009, Journal of dental research.

[24]  R. Oreffo,et al.  Osteoprogenitor response to semi-ordered and random nanotopographies. , 2006, Biomaterials.

[25]  W. Att,et al.  Ultraviolet light-mediated photofunctionalization of titanium to promote human mesenchymal stem cell migration, attachment, proliferation and differentiation. , 2009, Acta biomaterialia.

[26]  Matthew J Dalby,et al.  Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. , 2009, Acta biomaterialia.

[27]  Jin-Ming Wu,et al.  Large-scale preparation of ordered titania nanorods with enhanced photocatalytic activity. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[28]  Tejal A Desai,et al.  Influence of engineered titania nanotubular surfaces on bone cells. , 2007, Biomaterials.

[29]  Fanrong Pu,et al.  Effect of titanium carbide coating on the osseointegration response in vitro and in vivo. , 2007, Biomaterials.

[30]  Kaiyong Cai,et al.  Surface functionalized titanium thin films: zeta-potential, protein adsorption and cell proliferation. , 2006, Colloids and surfaces. B, Biointerfaces.

[31]  Chengtie Wu,et al.  Proliferation and osteoblastic differentiation of human bone marrow-derived stromal cells on akermanite-bioactive ceramics. , 2006, Biomaterials.

[32]  M. Pittenger,et al.  Multilineage potential of adult human mesenchymal stem cells. , 1999, Science.

[33]  S. Bauer,et al.  Another look at “Stem cell fate dictated solely by altered nanotube dimension” , 2009, Proceedings of the National Academy of Sciences.

[34]  J. Knowles,et al.  In vitro studies on the influence of surface modification of Ni-Ti alloy on human bone cells. , 2009, Journal of biomedical materials research. Part A.

[35]  J Lindström,et al.  Intra-osseous anchorage of dental prostheses. I. Experimental studies. , 1969, Scandinavian journal of plastic and reconstructive surgery.

[36]  B. Johanson,et al.  INTRA-OSSEOUS ANCHORAGE OF DENTAL PROSTHESES , 1970 .

[37]  Martin Schuler,et al.  Systematic study of osteoblast and fibroblast response to roughness by means of surface-morphology gradients. , 2007, Biomaterials.

[38]  Nikolaj Gadegaard,et al.  Nanotopographical control of human osteoprogenitor differentiation. , 2007, Current stem cell research & therapy.

[39]  Matthew J. Dalby,et al.  Whole proteome analysis of osteoprogenitor differentiation induced by disordered nanotopography and mediated by ERK signalling. , 2009, Biomaterials.

[40]  S. Hayakawa,et al.  Bioactive titania-gel layers formed by chemical treatment of Ti substrate with a H2O2/HCl solution. , 2002, Biomaterials.

[41]  Thomas J Webster,et al.  Increased osteoblast adhesion on nanophase metals: Ti, Ti6Al4V, and CoCrMo. , 2004, Biomaterials.

[42]  B. Nebe,et al.  Control of focal adhesion dynamics by material surface characteristics. , 2005, Biomaterials.

[43]  G W Marshall,et al.  Mechanical properties of human dental enamel on the nanometre scale. , 2001, Archives of oral biology.

[44]  K. Chattopadhyay,et al.  Controlling the surface topology and hence the hydrophobicity of amorphous carbon thin films , 2010 .

[45]  Mingce Long,et al.  Preparation of photocatalytic anatase nanowire films by in situ oxidation of titanium plate , 2009, Nanotechnology.

[46]  Robert Langer,et al.  New opportunities: the use of nanotechnologies to manipulate and track stem cells. , 2008, Cell stem cell.

[47]  Hongyi Li,et al.  Effects of TiO2 nanotubes with different diameters on gene expression and osseointegration of implants in minipigs. , 2011, Biomaterials.

[48]  W. Barthlott,et al.  Purity of the sacred lotus, or escape from contamination in biological surfaces , 1997, Planta.

[49]  A S G Curtis,et al.  Polymer-demixed nanotopography: control of fibroblast spreading and proliferation. , 2002, Tissue engineering.

[50]  D. Thierry,et al.  Variation of oxide films on titanium induced by osteoblast-like cell culture and the influence of an H2O2 pretreatment. , 1998, Journal of biomedical materials research.

[51]  T. Webster,et al.  Nanostructured biomaterials for tissue engineering bone. , 2007, Advances in biochemical engineering/biotechnology.

[52]  Myron Spector,et al.  Early bone apposition in vivo on plasma-sprayed and electrochemically deposited hydroxyapatite coatings on titanium alloy. , 2006, Biomaterials.

[53]  F. Guilak,et al.  Control of stem cell fate by physical interactions with the extracellular matrix. , 2009, Cell stem cell.

[54]  Fuzhai Cui,et al.  The biocompatibility of nanostructured calcium phosphate coated on micro-arc oxidized titanium. , 2008, Biomaterials.