Relative influence of surface topography and surface chemistry on cell response to bone implant materials. Part 2: Biological aspects

Abstract A current medical challenge is the replacement of tissue which can be thought of in terms of bone tissue engineering approaches. The key problem in bone tissue engineering lies in associating bone stem cells with material supports or scaffolds that can be implanted in a patient. Beside bone tissue engineering approaches, these types of materials are used daily in orthopaedics and dental practice as permanent or transitory implants such as ceramic bone filling materials or metallic prostheses. Consequently, it is essential to better understand how bone cells interact with materials. For several years, the current authors and others have developed in vitro studies in order to elucidate the mechanisms underlying the response of human bone cells to implant surfaces. This paper reviews the current state of knowledge and proposes future directions for research in this domain.

[1]  Maxence Bigerelle,et al.  Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. , 2000, Journal of biomedical materials research.

[2]  E. Bertolino,et al.  Transcriptional repression mediated by repositioning of genes to the nuclear lamina , 2008, Nature.

[3]  Ann-Sofie Andersson,et al.  Influence of systematically varied nanoscale topography on the morphology of epithelial cells , 2003, IEEE Transactions on NanoBioscience.

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

[5]  B D Boyan,et al.  Role of material surfaces in regulating bone and cartilage cell response. , 1996, Biomaterials.

[6]  A. Ruys,et al.  The influence of surface chemistry and topography on the contact guidance of MG63 osteoblast cells , 2007, Journal of materials science. Materials in medicine.

[7]  A S G Curtis,et al.  Investigating the limits of filopodial sensing: a brief report using SEM to image the interaction between 10 nm high nano‐topography and fibroblast filopodia , 2004, Cell biology international.

[8]  Nikolaj Gadegaard,et al.  Nanoprinting onto cells , 2006, Journal of The Royal Society Interface.

[9]  T. Kawai,et al.  Effect of microstructure of titanium surface on the behaviour of osteogenic cell line MC3T3-E1 , 1998, Journal of materials science. Materials in medicine.

[10]  D. Ingber,et al.  Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus , 2009, Nature Reviews Molecular Cell Biology.

[11]  Reinhard Schnettler,et al.  Comparison of new bone formation, implant integration, and biocompatibility between RGD-hydroxyapatite and pure hydroxyapatite coating for cementless joint prostheses--an experimental study in rabbits. , 2009, Journal of biomedical materials research. Part B, Applied biomaterials.

[12]  S. Ferguson,et al.  Potential of chemically modified hydrophilic surface characteristics to support tissue integration of titanium dental implants. , 2009, Journal of biomedical materials research. Part B, Applied biomaterials.

[13]  Ravi Dhurjati,et al.  Influence of substratum surface chemistry/energy and topography on the human fetal osteoblastic cell line hFOB 1.19: Phenotypic and genotypic responses observed in vitro. , 2007, Biomaterials.

[14]  W. Su,et al.  The geometric pattern of a pillared substrate influences the cell-process distribution and shapes of fibroblasts. , 2006, Micron.

[15]  Peter Fraser,et al.  Gene regulation through nuclear organization , 2007, Nature Structural &Molecular Biology.

[16]  T. Albrektsson,et al.  Qualitative and quantitative observations of bone tissue reactions to anodised implants. , 2002, Biomaterials.

[17]  B D Boyan,et al.  Surface roughness modulates the local production of growth factors and cytokines by osteoblast-like MG-63 cells. , 1996, Journal of biomedical materials research.

[18]  Jeffrey J. Fredberg,et al.  Universality in cell mechanics , 2008 .

[19]  A. Ben-Ze'ev,et al.  The cytoskeleton in cancer cells. , 1985, Biochimica et biophysica acta.

[20]  A Curtis,et al.  Synergistic and hierarchical adhesive and topographic guidance of BHK cells. , 1996, Experimental cell research.

[21]  M. Burger,et al.  Correlation between cell deformability and metastatic potential in B16-F1 melanoma cell variants. , 1988, Cancer research.

[22]  Masahiro Ohshima,et al.  Time-lapse observation of cell alignment on nanogrooved patterns , 2009, Journal of The Royal Society Interface.

[23]  Maxence Bigerelle,et al.  Role of materials surface topography on mammalian cell response , 2011 .

[24]  M. Hendzel,et al.  Mechanotransduction from the ECM to the genome: Are the pieces now in place? , 2008, Journal of cellular biochemistry.

[25]  David L. Cochran,et al.  Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. , 2003, European cells & materials.

[26]  P. Bongrand,et al.  Is there a predictable relationship between surface physical-chemical properties and cell behaviour at the interface? , 2004, European cells & materials.

[27]  B. Boyan,et al.  Surface roughness mediates its effects on osteoblasts via protein kinase A and phospholipase A2. , 1999, Biomaterials.

[28]  D Buser,et al.  What is This? Downloaded from jdr.sagepub.com at PENNSYLVANIA STATE UNIV on February 23, 2013 For personal use only. No other uses without permission. International and American Associations for Dental ResearchRESEARCH REPORTS , 2004 .

[29]  A. Lussi,et al.  Early loading of non-submerged titanium implants with a sandblasted and acid-etched surface. 5-year results of a prospective study in partially edentulous patients. , 2003, Clinical oral implants research.

[30]  Matthew J Dalby,et al.  Topographically induced direct cell mechanotransduction. , 2005, Medical engineering & physics.

[31]  M. Farina,et al.  Chemical and topographical influence of hydroxyapatite and beta-tricalcium phosphate surfaces on human osteoblastic cell behavior. , 2009, Journal of biomedical materials research. Part A.

[32]  L. Scheideler,et al.  Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. , 2006, Journal of biomedical materials research. Part A.

[33]  Maxence Bigerelle,et al.  Statistical correlation between cell adhesion and proliferation on biocompatible metallic materials. , 2005, Journal of biomedical materials research. Part A.

[34]  Thomas J Webster,et al.  Increased osteoblast adhesion on nanograined Ti modified with KRSR. , 2007, Journal of biomedical materials research. Part A.

[35]  Stefan Schinkinger,et al.  Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. , 2005, Biophysical journal.

[36]  U. Joos,et al.  Basic reactions of osteoblasts on structured material surfaces. , 2005, European cells & materials.

[37]  K. Anselme,et al.  Osteoblast adhesion on biomaterials. , 2000, Biomaterials.

[38]  Stefan Rammelt,et al.  Coating of titanium implants with collagen, RGD peptide and chondroitin sulfate. , 2006, Biomaterials.

[39]  Tejal A Desai,et al.  The effect of TiO2 nanotubes on endothelial function and smooth muscle proliferation. , 2009, Biomaterials.

[40]  B. Boyan,et al.  Surface roughness modulates the response of MG63 osteoblast-like cells to 1,25-(OH)(2)D(3) through regulation of phospholipase A(2) activity and activation of protein kinase A. , 1999, Journal of biomedical materials research.

[41]  Sungho Jin,et al.  Improved bone-forming functionality on diameter-controlled TiO(2) nanotube surface. , 2009, Acta biomaterialia.

[42]  Catherine D Reyes,et al.  The effect of integrin-specific bioactive coatings on tissue healing and implant osseointegration. , 2008, Biomaterials.

[43]  Patricia J Keely,et al.  Focal adhesion regulation of cell behavior. , 2004, Biochimica et biophysica acta.

[44]  M. Morra,et al.  Collagen I-coated titanium surfaces: mesenchymal cell adhesion and in vivo evaluation in trabecular bone implants. , 2006, Journal of biomedical materials research. Part A.

[45]  J. Jansen,et al.  Response of rat bone marrow cells to differently roughened titanium discs. , 1999, Clinical oral implants research.

[46]  T. Desai,et al.  Osteogenic differentiation of marrow stromal cells cultured on nanoporous alumina surfaces. , 2007, Journal of biomedical materials research. Part A.

[47]  Ali Othmane,et al.  Effect of surface topography and chemistry on adhesion, orientation and growth of fibroblasts on nickel–titanium substrates , 2002 .

[48]  D. Ingber,et al.  Cellular mechanotransduction: putting all the pieces together again , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[49]  David Boettiger,et al.  Effect of biomaterial surface properties on fibronectin-alpha5beta1 integrin interaction and cellular attachment. , 2006, Biomaterials.

[50]  Thomas J Webster,et al.  Nanobiotechnology: implications for the future of nanotechnology in orthopedic applications , 2004, Expert review of medical devices.

[51]  B. Boyan,et al.  Local factor production by MG63 osteoblast-like cells in response to surface roughness and 1,25-(OH)2D3 is mediated via protein kinase C- and protein kinase A-dependent pathways. , 2001, Biomaterials.

[52]  S. Ferguson,et al.  Biomechanical evaluation of the interfacial strength of a chemically modified sandblasted and acid-etched titanium surface. , 2006, Journal of biomedical materials research. Part A.

[53]  Effect of a gold–palladium coating on the long-term adhesion of human osteoblasts on biocompatible metallic materials , 2006 .

[54]  D. Ingber.  Tensegrity: the architectural basis of cellular mechanotransduction. , 1997, Annual review of physiology.

[55]  M G Ehrlich,et al.  RGD-coated titanium implants stimulate increased bone formation in vivo. , 1999, Biomaterials.

[56]  J. Jacobs,et al.  Evaluation of metallic and polymeric biomaterial surface energy and surface roughness characteristics for directed cell adhesion. , 2001, Tissue engineering.

[57]  D. Deligianni,et al.  Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. , 2001, Biomaterials.

[58]  B. Boyan,et al.  Requirement for both micron- and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography. , 2007, Biomaterials.

[59]  J. Nebe,et al.  Interface interactions of osteoblasts with structured titanium and the correlation between physicochemical characteristics and cell biological parameters. , 2007, Macromolecular bioscience.

[60]  E. Vogler,et al.  Systematic variation in osteoblast adhesion and phenotype with substratum surface characteristics. , 2004, Journal of biomedical materials research. Part A.

[61]  Douglas W Hamilton,et al.  Comparative response of epithelial cells and osteoblasts to microfabricated tapered pit topographies in vitro and in vivo. , 2007, Biomaterials.

[62]  H. Toutenburg,et al.  Stability change of chemically modified sandblasted/acid-etched titanium palatal implants. A randomized-controlled clinical trial. , 2009, Clinical oral implants research.

[63]  D. Hamilton,et al.  The effect of substratum topography on osteoblast adhesion mediated signal transduction and phosphorylation. , 2007, Biomaterials.

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

[65]  Matthew C. Phipps,et al.  The effect of RGD peptides on osseointegration of hydroxyapatite biomaterials. , 2008, Biomaterials.

[66]  B. Boyan,et al.  Integrin α2β1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates , 2008, Proceedings of the National Academy of Sciences.

[67]  W. Soboyejo,et al.  Cell/surface interactions and adhesion on Ti-6Al-4V: effects of surface texture. , 2007, Journal of biomedical materials research. Part B, Applied biomaterials.

[68]  T. Albrektsson,et al.  Bone reaction to nano hydroxyapatite modified titanium implants placed in a gap-healing model. , 2008, Journal of biomedical materials research. Part A.

[69]  Ralf J Kohal,et al.  The gene-expression and phenotypic response of hFOB 1.19 osteoblasts to surface-modified titanium and zirconia. , 2009, Biomaterials.

[70]  Yang Leng,et al.  Quantitative analysis of osteoblast behavior on microgrooved hydroxyapatite and titanium substrata. , 2003, Journal of biomedical materials research. Part A.

[71]  J. Jansen,et al.  Implant Surface Roughness and Bone Healing: a Systematic Review , 2006, Journal of dental research.

[72]  Maxence Bigerelle,et al.  The relative influence of the topography and chemistry of TiAl6V4 surfaces on osteoblastic cell behaviour. , 2000, Biomaterials.

[73]  Kenneth M. Yamada,et al.  Cell interactions with three-dimensional matrices. , 2002, Current opinion in cell biology.

[74]  A. Sewing,et al.  Tools for tissue engineering of mineralized oral structures , 2000, Clinical Oral Investigations.

[75]  B. Ratner,et al.  Fibrinogen adsorption, platelet adhesion and activation on mixed hydroxyl-/methyl-terminated self-assembled monolayers. , 2006, Biomaterials.

[76]  S. Affrossman,et al.  Cell response to nano-islands produced by polymer demixing: a brief review. , 2004, IEE proceedings. Nanobiotechnology.

[77]  C. Gay-Escoda,et al.  In vivo low-density bone apposition on different implant surface materials. , 2009, International journal of oral and maxillofacial surgery.

[78]  Joshua C. Hansen,et al.  The regulation of integrin-mediated osteoblast focal adhesion and focal adhesion kinase expression by nanoscale topography. , 2007, Biomaterials.

[79]  T. Webster,et al.  Mechanisms of enhanced osteoblast adhesion on nanophase alumina involve vitronectin. , 2001, Tissue engineering.

[80]  D. Landolt,et al.  Time-dependent morphology and adhesion of osteoblastic cells on titanium model surfaces featuring scale-resolved topography. , 2004, Biomaterials.

[81]  A. Wennerberg,et al.  Bone formation at titanium implants prepared with iso- and anisotropic surfaces of similar roughness: an in vivo study. , 2005, Clinical implant dentistry and related research.

[82]  Thomas J Webster,et al.  Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. , 2006, Journal of biomedical materials research. Part A.

[83]  P. Campbell,et al.  Variation in surface texture measurements. , 2004, Journal of biomedical materials research. Part B, Applied biomaterials.

[84]  Benjamin G. Keselowsky,et al.  Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[85]  M. Tonetti,et al.  Roughness response genes in osteoblasts. , 2004, Bone.

[86]  J. van den Dolder,et al.  Influence of RGD-loaded titanium implants on bone formation in vivo. , 2005, Tissue engineering.

[87]  Nikolaj Gadegaard,et al.  Investigating filopodia sensing using arrays of defined nano-pits down to 35 nm diameter in size. , 2004, The international journal of biochemistry & cell biology.

[88]  T. Albrektsson,et al.  Oxidized titanium screws coated with calcium ions and their performance in rabbit bone. , 2002, The International journal of oral & maxillofacial implants.

[89]  H. Kessler,et al.  Cellular unbinding forces of initial adhesion processes on nanopatterned surfaces probed with magnetic tweezers. , 2006, Nano letters.

[90]  C. Werner,et al.  Self-assembled monolayers with different terminating groups as model substrates for cell adhesion studies. , 2004, Biomaterials.

[91]  F Rupp,et al.  High surface energy enhances cell response to titanium substrate microstructure. , 2005, Journal of biomedical materials research. Part A.

[92]  T. Albrektsson,et al.  Nano hydroxyapatite structures influence early bone formation. , 2008, Journal of biomedical materials research. Part A.

[93]  Jean-Pierre Bernard,et al.  The use of reduced healing times on ITI implants with a sandblasted and acid-etched (SLA) surface: early results from clinical trials on ITI SLA implants. , 2002, Clinical oral implants research.

[94]  M. Alexander,et al.  Investigation of cell-surface interactions using chemical gradients formed from plasma polymers. , 2008, Biomaterials.

[95]  F. Goubard,et al.  Kinetics of conformational changes of fibronectin adsorbed onto model surfaces. , 2008, Colloids and surfaces. B, Biointerfaces.

[96]  M. Biggs,et al.  Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330 nm deep microgrooves , 2008, Journal of The Royal Society Interface.

[97]  S. Bellis,et al.  Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. , 2001, Journal of biomedical materials research.

[98]  B. Boyan,et al.  Integrin beta1 silencing in osteoblasts alters substrate-dependent responses to 1,25-dihydroxy vitamin D3. , 2006, Biomaterials.

[99]  Maxence Bigerelle,et al.  Statistical demonstration of the relative effect of surface chemistry and roughness on human osteoblast short-term adhesion , 2006, Journal of materials science. Materials in medicine.

[100]  C. R. Howlett,et al.  Effect of surface chemical modification of bioceramic on phenotype of human bone-derived cells. , 1999, Journal of biomedical materials research.

[101]  Pedro Madureira,et al.  The influence of functional groups of self-assembled monolayers on fibrous capsule formation and cell recruitment. , 2006, Journal of biomedical materials research. Part A.

[102]  Maxence Bigerelle,et al.  Topography effects of pure titanium substrates on human osteoblast long-term adhesion. , 2005, Acta biomaterialia.

[103]  C. Lohmann,et al.  Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. , 1998, Biomaterials.

[104]  M. Beloti,et al.  Rat bone marrow cell response to titanium and titanium alloy with different surface roughness. , 2003, Clinical oral implants research.

[105]  V. Hasırcı,et al.  Microstructured Surfaces Cause Severe but Non‐Detrimental Deformation of the Cell Nucleus , 2009 .

[106]  Benjamin Geiger,et al.  Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. , 2008, Nano letters.

[107]  T. Webster,et al.  Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. , 2000, Journal of biomedical materials research.

[108]  Maxence Bigerelle,et al.  Improvement in the morphology of Ti-based surfaces: a new process to increase in vitro human osteoblast response. , 2002, Biomaterials.

[109]  F. He,et al.  Early bone response to sandblasted, dual acid-etched and H2O2/HCl treated titanium implants: an experimental study in the rabbit. , 2009, International journal of oral and maxillofacial surgery.

[110]  Andrés J. García,et al.  Biomolecular surface coating to enhance orthopaedic tissue healing and integration. , 2007, Biomaterials.

[111]  S. Thompson,et al.  Hyperpolarizing responses to stretch in sensory neurones innervating leech body wall muscle. , 1988, The Journal of physiology.

[112]  A Wennerberg,et al.  Determining optimal surface roughness of TiO(2) blasted titanium implant material for attachment, proliferation and differentiation of cells derived from human mandibular alveolar bone. , 2001, Clinical oral implants research.

[113]  Sandra Downes,et al.  Protein adsorption and human osteoblast-like cell attachment and growth on alkylthiol on gold self-assembled monolayers. , 2002, Journal of biomedical materials research.

[114]  P S Walker,et al.  Attachment and proliferation of osteoblasts and fibroblasts on biomaterials for orthopaedic use. , 1995, Biomaterials.

[115]  Tejal A Desai,et al.  Titania nanotubes: a novel platform for drug-eluting coatings for medical implants? , 2007, Small.

[116]  D R McKenzie,et al.  Effect of ion modification of commonly used orthopedic materials on the attachment of human bone-derived cells. , 1999, Journal of biomedical materials research.

[117]  Karine Anselme,et al.  Topographically induced self-deformation of the nuclei of cells: dependence on cell type and proposed mechanisms , 2010, Journal of materials science. Materials in medicine.

[118]  L. Postiglione,et al.  Different titanium surfaces modulate the bone phenotype of SaOS-2 osteoblast-like cells. , 2004, European journal of histochemistry : EJH.

[119]  T. Webster,et al.  Nanometer surface roughness increases select osteoblast adhesion on carbon nanofiber compacts. , 2004, Journal of biomedical materials research. Part A.

[120]  Huipin Yuan,et al.  3D microenvironment as essential element for osteoinduction by biomaterials. , 2005, Biomaterials.

[121]  L F Cooper,et al.  A role for surface topography in creating and maintaining bone at titanium endosseous implants. , 2000, The Journal of prosthetic dentistry.

[122]  L. Bonewald,et al.  Maturation State Determines the Response of Osteogenic Cells to Surface Roughness and 1,25‐Dihydroxyvitamin D3 , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[123]  M. Morra,et al.  Surface engineering of titanium by collagen immobilization. Surface characterization and in vitro and in vivo studies. , 2003, Biomaterials.

[124]  B. Nebe,et al.  Cell-extracellular matrix interaction and physico-chemical characteristics of titanium surfaces depend on the roughness of the material. , 2002, Biomolecular engineering.

[125]  E. Leite,et al.  Nanostructured alumina-coated implant surface: effect on osteoblast-related gene expression and bone-to-implant contact in vivo. , 2009, The International journal of oral & maxillofacial implants.

[126]  J. Planell,et al.  Spatial organization of osteoblast fibronectin matrix on titanium surfaces: effects of roughness, chemical heterogeneity and surface energy. , 2010, Acta biomaterialia.

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

[128]  A. Nanci,et al.  Enhancement of in vitro osteogenesis on titanium by chemically produced nanotopography. , 2007, Journal of biomedical materials research. Part A.

[129]  D. Brunette,et al.  The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. , 1999, Journal of biomechanical engineering.

[130]  J. Jansen,et al.  The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion. , 2007, Biomaterials.

[131]  R E Baier,et al.  Surface properties determine bioadhesive outcomes: methods and results. , 1984, Journal of biomedical materials research.

[132]  Cameron J Wilson,et al.  Mediation of biomaterial-cell interactions by adsorbed proteins: a review. , 2005, Tissue engineering.

[133]  N. Jaffrezic‐Renault,et al.  Biomaterial surface properties modulate in vitro rat calvaria osteoblasts response: Roughness and or chemistry? , 2008 .

[134]  Maxence Bigerelle,et al.  Modelling approach in cell/material interactions studies. , 2006, Biomaterials.

[135]  T. Webster,et al.  Enhanced functions of osteoblasts on nanophase ceramics. , 2000, Biomaterials.

[136]  B. Boyan,et al.  Response of normal female human osteoblasts (NHOst) to 17beta-estradiol is modulated by implant surface morphology. , 2002, Journal of biomedical materials research.

[137]  T. Webster,et al.  Selective bone cell adhesion on formulations containing carbon nanofibers. , 2003, Biomaterials.

[138]  J. Amédée,et al.  Effect of surface roughness of the titanium alloy Ti-6Al-4V on human bone marrow cell response and on protein adsorption. , 2001, Biomaterials.

[139]  In-Seop Lee,et al.  The biocompatibility of SLA-treated titanium implants , 2008, Biomedical materials.

[140]  Maxence Bigerelle,et al.  Effect of grooved titanium substratum on human osteoblastic cell growth. , 2002, Journal of biomedical materials research.

[141]  A Curtis,et al.  Topographical control of cells. , 1997, Biomaterials.

[142]  J. Davies,et al.  Bone bonding at natural and biomaterial surfaces. , 2007, Biomaterials.

[143]  Matthew J Dalby,et al.  Fibroblast response to a controlled nanoenvironment produced by colloidal lithography. , 2004, Journal of biomedical materials research. Part A.

[144]  H. Busscher,et al.  The influence of substratum surface free energy on growth and spreading of human fibroblasts in the presence and absence of serum proteins. , 1986, Journal of biomedical materials research.

[145]  U. Ripamonti.  Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. , 1996, Biomaterials.

[146]  B. Boyan,et al.  Titanium surface roughness alters responsiveness of MG63 osteoblast‐like cells to 1α,25‐(OH)2D3 , 1998 .

[147]  B D Boyan,et al.  Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). , 1995, Journal of biomedical materials research.

[148]  R. Tuan,et al.  Regulation of human osteoblast integrin expression by orthopedic implant materials. , 1996, Bone.

[149]  Maxence Bigerelle,et al.  An unscaled parameter to measure the order of surfaces: a new surface elaboration to increase cells adhesion. , 2002, Biomolecular engineering.

[150]  Daniel A Starr.  A nuclear-envelope bridge positions nuclei and moves chromosomes , 2009, Journal of Cell Science.

[151]  J. Heath,et al.  A new hypothesis of contact guidance in tissue cells. , 1976, Experimental cell research.

[152]  M. Titus,et al.  Myosins: matching functions with motors. , 1998, Current opinion in cell biology.

[153]  G. Truskey,et al.  Effect of the conformation and orientation of adsorbed fibronectin on endothelial cell spreading and the strength of adhesion. , 1993, Journal of biomedical materials research.

[154]  C. Wilkinson,et al.  The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. , 2007, Nature materials.

[155]  B. Boyan,et al.  Integrin alpha(5) controls osteoblastic proliferation and differentiation responses to titanium substrates presenting different roughness characteristics in a roughness independent manner. , 2007, Journal of biomedical materials research. Part A.

[156]  Felix Beckmann,et al.  Osteoconductive modifications of Ti-implants in a goat defect model: characterization of bone growth with SR muCT and histology. , 2005, Biomaterials.

[157]  Kjeld Søballe,et al.  In vivo study of the effect of RGD treatment on bone ongrowth on press-fit titanium alloy implants. , 2005, Biomaterials.

[158]  T. Albrektsson,et al.  The roles of surface chemistry and topography in the strength and rate of osseointegration of titanium implants in bone. , 2009, Journal of biomedical materials research. Part A.

[159]  Marco Wieland,et al.  Mechanisms regulating increased production of osteoprotegerin by osteoblasts cultured on microstructured titanium surfaces. , 2009, Biomaterials.

[160]  J. Jansen,et al.  Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. , 2005, Biomaterials.

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

[162]  Joong Yull Park,et al.  Study of cellular behaviors on concave and convex microstructures fabricated from elastic PDMS membranes. , 2009, Lab on a chip.

[163]  Thomas J Webster,et al.  Endothelial and vascular smooth muscle cell function on poly(lactic-co-glycolic acid) with nano-structured surface features. , 2004, Biomaterials.

[164]  P Ducheyne,et al.  Bioactive ceramics: the effect of surface reactivity on bone formation and bone cell function. , 1999, Biomaterials.

[165]  U. Joos,et al.  Influence of titanium surfaces on attachment of osteoblast-like cells in vitro. , 2004, Biomaterials.

[166]  J. Nebe,et al.  The influence of surface roughness of titanium on β1- and β3-integrin adhesion and the organization of fibronectin in human osteoblastic cells , 2005 .

[167]  M. Anpo,et al.  The effect of ultraviolet functionalization of titanium on integration with bone. , 2009, Biomaterials.

[168]  Adam W Feinberg,et al.  Systematic variation of microtopography, surface chemistry and elastic modulus and the state dependent effect on endothelial cell alignment. , 2008, Journal of biomedical materials research. Part A.

[169]  Xing‐dong Zhang,et al.  Osteoinduction by calcium phosphate biomaterials , 1998, Journal of materials science. Materials in medicine.

[170]  David L. Cochran,et al.  Mechanisms Involved in Osteoblast Response to Implant Surface Morphology , 2001 .

[171]  T. Albrektsson,et al.  Bone reactions to oxidized titanium implants with electrochemical anion sulphuric acid and phosphoric acid incorporation. , 2002, Clinical implant dentistry and related research.

[172]  Pedro Moreo,et al.  On the effect of substrate curvature on cell mechanics. , 2009, Biomaterials.

[173]  M. Harmand,et al.  Study of the effect of the surface state on the cytocompatibility of a Co-Cr alloy using human osteoblasts and fibroblasts. , 1990, Journal of biomedical materials research.

[174]  Joachim P Spatz,et al.  Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly. , 2006, European journal of cell biology.

[175]  H. Busscher,et al.  Amount and surface structure of albumin adsorbed to solid substrata with different wettabilities in a parallel plate flow cell. , 1990, Journal of biomedical materials research.

[176]  Tejal A Desai,et al.  Fabrication and evaluation of nanoporous alumina membranes for osteoblast culture. , 2005, Journal of biomedical materials research. Part A.

[177]  T. Webster,et al.  PLGA nanometer surface features manipulate fibronectin interactions for improved vascular cell adhesion. , 2007, Journal of biomedical materials research. Part A.

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

[179]  Xing‐dong Zhang,et al.  Bone morphogenetic protein and ceramic-induced osteogenesis , 1998, Journal of materials science. Materials in medicine.

[180]  Thomas Jay Webster,et al.  Nanomedicine for implants: a review of studies and necessary experimental tools. , 2007, Biomaterials.

[181]  Besim Ben Nissan,et al.  The effect of surface chemistry modification of titanium alloy on signalling pathways in human osteoblasts. , 2005, Biomaterials.