The interaction of cells and bacteria with surfaces structured at the nanometre scale.

The current development of nanobiotechnologies requires a better understanding of cell-surface interactions on the nanometre scale. Recently, advances in nanoscale patterning and detection have allowed the fabrication of appropriate substrates and the study of cell-substrate interactions. In this review we discuss the methods currently available for nanoscale patterning and their merits, as well as techniques for controlling the surface chemistry of materials at the nanoscale without changing the nanotopography and the possibility of truly characterizing the surface chemistry at the nanoscale. We then discuss the current knowledge of how a cell can interact with a substrate at the nanoscale and the effect of size, morphology, organization and separation of nanofeatures on cell response. Moreover, cell-substrate interactions are mediated by the presence of proteins adsorbed from biological fluids on the substrate. Many questions remain on the effect of nanotopography on protein adsorption. We review papers related to this point. As all these parameters have an influence on cell response, it is important to develop specific studies to point out their relative influence, as well as the biological mechanisms underlying cell responses to nanotopography. This will be the basis for future research in this field. An important topic in tissue engineering is the effect of nanoscale topography on bacteria, since cells have to compete with bacteria in many environments. The limited current knowledge of this topic is also discussed in the light of using topography to encourage cell adhesion while limiting bacterial adhesion. We also discuss current and prospective applications of cell-surface interactions on the nanoscale. Finally, based on questions raised previously that remain to be solved in the field, we propose future directions of research in materials science to help elucidate the relative influence of the physical and chemical aspects of nanotopography on bacteria and cell response with the aim of contributing to the development of nanobiotechnologies.

[1]  S. Hajati,et al.  XPS imaging of depth profiles and amount of substance based on Tougaard’s algorithm , 2006 .

[2]  Martin Bastmeyer,et al.  Cell behaviour on micropatterned substrata: limits of extracellular matrix geometry for spreading and adhesion , 2004, Journal of Cell Science.

[3]  Klaus Affeld,et al.  The effect of surface roughness on activation of the coagulation system and platelet adhesion in rotary blood pumps. , 2007, Artificial organs.

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

[5]  C. Wilkinson,et al.  New depths in cell behaviour: reactions of cells to nanotopography. , 1999, Biochemical Society symposium.

[6]  B. Smets,et al.  Surface physicochemical properties of Pseudomonas fluorescens and impact on adhesion and transport through porous media , 1999 .

[7]  Duncan S Sutherland,et al.  In vitro and in vivo response to nanotopographically-modified surfaces of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) and polycaprolactone , 2006, Journal of biomaterials science. Polymer edition.

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

[9]  John C. Vickerman,et al.  Surface analysis : the principal techniques , 2009 .

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

[11]  Lars Rasmusson,et al.  Titanium dioxide nanotubes enhance bone bonding in vivo. , 2009, Journal of biomedical materials research. Part A.

[12]  Yang Cheng,et al.  Is the lotus leaf superhydrophobic , 2005 .

[13]  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.

[14]  Takeshi Ito,et al.  Newly Developed Chemical Probes and Nano-Devices for Cellular Analysis , 2008, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[15]  Julie Gold,et al.  Protein Adsorption on Model Surfaces with Controlled Nanotopography and Chemistry , 2002 .

[16]  Matthew J Dalby,et al.  Use of nanotopography to study mechanotransduction in fibroblasts--methods and perspectives. , 2004, European journal of cell biology.

[17]  Tejal A Desai,et al.  Nanostructured antifouling poly(ethylene glycol) films for silicon-based microsystems. , 2005, Journal of nanoscience and nanotechnology.

[18]  M. Hamilton,et al.  Effects of Substratum Topography on Bacterial Adhesion. , 1998, Journal of colloid and interface science.

[19]  Ravi S Kane,et al.  Nanobiotechnology: Protein‐Nanomaterial Interactions , 2007, Biotechnology progress.

[20]  P. Smethurst,et al.  Identification in Collagen Type I of an Integrin α2β1-binding Site Containing an Essential GER Sequence* , 1998, The Journal of Biological Chemistry.

[21]  L. Murr,et al.  Cytotoxic effects of aggregated nanomaterials. , 2007, Acta biomaterialia.

[22]  A. Rutenberg,et al.  Microbial response to surface microtopography: the role of metabolism in localized mineral dissolution , 2001 .

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

[24]  R. Bruce Lennox,et al.  Patterned surfaces via self-assembly , 1999 .

[25]  Yong Wang,et al.  Adhesion and proliferation of OCT-1 osteoblast-like cells on micro- and nano-scale topography structured poly(L-lactide). , 2005, Biomaterials.

[26]  R G Richards,et al.  Staphylococcus aureus adhesion to different treated titanium surfaces , 2004, Journal of materials science. Materials in medicine.

[27]  H. Solak,et al.  Nanopatterns with biological functions. , 2006, Journal of nanoscience and nanotechnology.

[28]  Maryam Tabrizian,et al.  Cellular and molecular interactions between MC3T3-E1 pre-osteoblasts and nanostructured titanium produced by high-pressure torsion. , 2007, Biomaterials.

[29]  H. Vaudry,et al.  Proteomic comparison of outer membrane protein patterns of sessile and planktonic Pseudomonas aeruginosa cells , 2005 .

[30]  F. Bäckhed,et al.  Nanoscale features influence epithelial cell morphology and cytokine production. , 2003, Biomaterials.

[31]  R. Funk,et al.  Effects of Different Titanium Alloys and Nanosize Surface Patterning on Adhesion, Differentiation, and Orientation of Osteoblast-Like Cells , 2005, Cells Tissues Organs.

[32]  D. Campoccia,et al.  Study of Staphylococcus Aureus Adhesion on a Novel Nanostructured Surface by Chemiluminometry , 2006, The International journal of artificial organs.

[33]  Thomas J Webster,et al.  The relationship between the nanostructure of titanium surfaces and bacterial attachment. , 2010, Biomaterials.

[34]  Nancy L Allbritton,et al.  CRITICAL REVIEW www.rsc.org/loc | Lab on a Chip Analysis of single mammalian cells on-chip , 2006 .

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

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

[37]  C. Michiels,et al.  Role of bacterial cell surface structures in Escherichia coli biofilm formation. , 2005, Research in microbiology.

[38]  L. Barnes,et al.  Effect of Milk Proteins on Adhesion of Bacteria to Stainless Steel Surfaces , 1999, Applied and Environmental Microbiology.

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

[40]  Joachim P Spatz,et al.  Protein repellent properties of covalently attached PEG coatings on nanostructured SiO(2)-based interfaces. , 2007, Biomaterials.

[41]  D. Grant,et al.  The effect of surface chemistry and nanotopography of titanium nitride (TiN) films on 3T3-L1 fibroblasts. , 2003, Journal of biomedical materials research. Part A.

[42]  K E Healy,et al.  The role of vitronectin in the attachment and spatial distribution of bone-derived cells on materials with patterned surface chemistry. , 1997, Journal of biomedical materials research.

[43]  F. Rossi,et al.  Surface Functionalization and Patterning Techniques to Design Interfaces for Biomedical and Biosensor Applications , 2006 .

[44]  R. Lennox,et al.  Self-Assembled Masks for the Transfer of Nanometer-Scale Patterns into Surfaces: Characterization by AFM and LFM , 2002 .

[45]  Nanostructured magnetizable materials that switch cells between life and death. , 2007, Biomaterials.

[46]  R. Oreffo,et al.  The interaction of human bone marrow cells with nanotopographical features in three dimensional constructs. , 2006, Journal of biomedical materials research. Part A.

[47]  L. Schlapbach,et al.  Protein adsorption on topographically nanostructured titanium , 2001 .

[48]  Song Xu,et al.  Nanofabrication of self-assembled monolayers using scanning probe lithography. , 2000, Accounts of chemical research.

[49]  F. Stellacci,et al.  Contact Printing Beyond Surface Roughness: Liquid Supramolecular Nanostamping , 2007 .

[50]  K. Komvopoulos,et al.  Differential regulation of endothelial cell adhesion, spreading, and cytoskeleton on low-density polyethylene by nanotopography and surface chemistry modification induced by argon plasma treatment. , 2008, Journal of biomedical materials research. Part A.

[51]  R. Kolter,et al.  Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili , 1998, Molecular microbiology.

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

[53]  S. Ramakrishna,et al.  A review on electrospinning design and nanofibre assemblies , 2006, Nanotechnology.

[54]  K J Stout,et al.  Development of methods for the characterisation of roughness in three dimensions , 2000 .

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

[56]  X. F. Wang,et al.  Nanoscale surface topography enhances cell adhesion and gene expression of madine darby canine kidney cells , 2008, Journal of materials science. Materials in medicine.

[57]  W. Frey,et al.  Nanopatterning of fibronectin and the influence of integrin clustering on endothelial cell spreading and proliferation. , 2008, Journal of biomedical materials research. Part A.

[58]  John D. Brooks,et al.  Properties of the stainless steel substrate, influencing the adhesion of thermo-resistant streptococci , 2000 .

[59]  M. Garcia-Parajo,et al.  Selective Immobilization of Protein Clusters on Polymeric Nanocraters , 2006 .

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

[61]  Ann-Sofie Andersson,et al.  The effects of continuous and discontinuous groove edges on cell shape and alignment. , 2003, Experimental cell research.

[62]  A. Curtis,et al.  Human Fibroblast and Human Bone Marrow Cell Response to Lithographically Nanopatterned Adhesive Domains on Protein Rejecting Substrates , 2007, IEEE Transactions on NanoBioscience.

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

[64]  Benjamin M. Wu,et al.  Cell interaction with three-dimensional sharp-tip nanotopography. , 2007, Biomaterials.

[65]  M. Nardin,et al.  Quantitative and morphological analysis of biofilm formation on self-assembled monolayers. , 2007, Colloids and surfaces. B, Biointerfaces.

[66]  S. Aota,et al.  The short amino acid sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. , 1994, The Journal of biological chemistry.

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

[68]  C. Murphy,et al.  Responses of human keratocytes to micro- and nanostructured substrates. , 2004, Journal of biomedical materials research. Part A.

[69]  S. Ramakrishna,et al.  Applications of polymer nanofibers in biomedicine and biotechnology , 2005, Applied biochemistry and biotechnology.

[70]  J. Spatz,et al.  Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. , 2009, Acta biomaterialia.

[71]  Gangyao Wen,et al.  Effect of spreading solvents on Langmuir monolayers and Langmuir–Blodgett films of PS-b-P2VP , 2006 .

[72]  Sarah Kim,et al.  Nanomachining by colloidal lithography. , 2006, Small.

[73]  B. Rezek,et al.  Strong influence of hierarchically structured diamond nanotopography on adhesion of human osteoblasts and mesenchymal cells , 2009 .

[74]  Gabriela Kalna,et al.  Nanotopographical stimulation of mechanotransduction and changes in interphase centromere positioning , 2007, Journal of cellular biochemistry.

[75]  Neil A. Anderson,et al.  Nanoscale optical imaging of single-walled carbon nanotubes , 2006 .

[76]  C. Murphy,et al.  Epithelial contact guidance on well-defined micro- and nanostructured substrates , 2003, Journal of Cell Science.

[77]  G. Forgacs On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. , 1995, Journal of cell science.

[78]  C J Murphy,et al.  Nanoscale topography modulates corneal epithelial cell migration. , 2003, Journal of biomedical materials research. Part A.

[79]  R. Salvarezza,et al.  Nano/microscale order affects the early stages of biofilm formation on metal surfaces. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[80]  K. Otto,et al.  Adhesion of Type 1-Fimbriated Escherichia coli to Abiotic Surfaces Leads to Altered Composition of Outer Membrane Proteins , 2001, Journal of bacteriology.

[81]  Chad A Mirkin,et al.  The evolution of dip-pen nanolithography. , 2004, Angewandte Chemie.

[82]  A S G Curtis,et al.  Fibroblast reaction to island topography: changes in cytoskeleton and morphology with time. , 2003, Biomaterials.

[83]  Hee‐Tae Jung,et al.  Application of supramolecular nanostamping to the replication of DNA nanoarrays. , 2007, Nano letters.

[84]  Jeen-Shang Lin,et al.  Mechanoregulation of gene expression in fibroblasts. , 2007, Gene.

[85]  S. Krishnamoorthy,et al.  Tuning the Dimensions and Periodicities of Nanostructures Starting from the Same Polystyrene‐block‐poly(2‐vinylpyridine) Diblock Copolymer , 2006 .

[86]  Byungkyu Kim,et al.  Label-free, microfluidic separation and enrichment of human breast cancer cells by adhesion difference. , 2007, Lab on a chip.

[87]  E. Amanatides,et al.  Staphylococcus epidermidis adhesion to He, He/O(2) plasma treated PET films and aged materials: contributions of surface free energy and shear rate. , 2008, Colloids and surfaces. B, Biointerfaces.

[88]  Sungho Jin,et al.  Significantly accelerated osteoblast cell growth on aligned TiO2 nanotubes. , 2006, Journal of biomedical materials research. Part A.

[89]  E. Ivanova,et al.  Differences in colonisation of five marine bacteria on two types of glass surfaces , 2009, Biofouling.

[90]  M. Wood Colloidal lithography and current fabrication techniques producing in-plane nanotopography for biological applications , 2007, Journal of The Royal Society Interface.

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

[92]  A. Kromka,et al.  Study on cellular adhesion of human osteoblasts on nano‐structured diamond films , 2009 .

[93]  Micro- and nanopatterned star poly(ethylene glycol) (PEG) materials prepared by UV-based imprint lithography. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[94]  Julie Gold,et al.  Quantitative assessment of the response of primary derived human osteoblasts and macrophages to a range of nanotopography surfaces in a single culture model in vitro. , 2003, Biomaterials.

[95]  J. Jansen,et al.  Early spreading events of fibroblasts on microgrooved substrates. , 2000, Journal of biomedical materials research.

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

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

[98]  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.

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

[100]  A S G Curtis,et al.  In vitro reaction of endothelial cells to polymer demixed nanotopography. , 2002, Biomaterials.

[101]  P. Bagnaninchi,et al.  The beta integrins and cytoskeletal nanoimprinting. , 2008, Experimental cell research.

[102]  Marcus Textor,et al.  A Novel Approach to Produce Protein Nanopatterns by Combining Nanoimprint Lithography and Molecular Self-Assembly , 2004 .

[103]  J. Planell,et al.  Focused ion beam/scanning electron microscopy characterization of cell behavior on polymer micro-/nanopatterned substrates: a study of cell-substrate interactions. , 2008, Micron.

[104]  R Geoff Richards,et al.  The use of nanoscale topography to modulate the dynamics of adhesion formation in primary osteoblasts and ERK/MAPK signalling in STRO-1+ enriched skeletal stem cells. , 2009, Biomaterials.

[105]  Joachim P Spatz,et al.  Activation of integrin function by nanopatterned adhesive interfaces. , 2004, Chemphyschem : a European journal of chemical physics and physical chemistry.

[106]  E. Baker,et al.  Pili in Gram-negative and Gram-positive bacteria — structure, assembly and their role in disease , 2009, Cellular and Molecular Life Sciences.

[107]  K. Nguyen,et al.  Cellular and molecular responses of smooth muscle cells to surface nanotopography. , 2007, Journal of nanoscience and nanotechnology.

[108]  É. Bertrand,et al.  Subcellular proteomics : from cell deconstruction to system reconstruction , 2007 .

[109]  John Q. Trojanowski,et al.  Single-Cell Gene Expression Analysis: Implications for Neurodegenerative and Neuropsychiatric Disorders , 2004, Neurochemical Research.

[110]  A. Curtis,et al.  Attempted endocytosis of nano-environment produced by colloidal lithography by human fibroblasts. , 2004, Experimental cell research.

[111]  Janos Vörös,et al.  Systematic study of osteoblast response to nanotopography by means of nanoparticle-density gradients. , 2007, Biomaterials.

[112]  Roberto Kolter,et al.  Biofilms: the matrix revisited. , 2005, Trends in microbiology.

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

[114]  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.

[115]  Loïc J Blum,et al.  Enzyme association with lipidic Langmuir-Blodgett films: interests and applications in nanobioscience. , 2005, Advances in colloid and interface science.

[116]  A. Curtis,et al.  Rapid fibroblast adhesion to 27nm high polymer demixed nano-topography. , 2004, Biomaterials.

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

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

[119]  Seeram Ramakrishna,et al.  Electrospun scaffold tailored for tissue‐specific extracellular matrix , 2006, Biotechnology journal.

[120]  V. Shastri,et al.  The effect of silica nanoparticle-modified surfaces on cell morphology, cytoskeletal organization and function. , 2008, Biomaterials.

[121]  Joshua C. Hansen,et al.  Osteoblast adhesion on poly(L-lactic acid)/polystyrene demixed thin film blends: effect of nanotopography, surface chemistry, and wettability. , 2005, Biomacromolecules.

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

[123]  C. Kirkpatrick,et al.  Functionality of endothelial cells on silk fibroin nets: comparative study of micro- and nanometric fibre size. , 2008, Biomaterials.

[124]  W. Nisch,et al.  Variation in contact guidance by human cells on a microstructured surface. , 1995, Journal of biomedical materials research.

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

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

[127]  Newell R Washburn,et al.  High-throughput investigation of osteoblast response to polymer crystallinity: influence of nanometer-scale roughness on proliferation. , 2004, Biomaterials.

[128]  The effect of surface chemistry and nanotopography of titanium nitride (TiN) films on primary hippocampal neurones. , 2004, Biomaterials.

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

[130]  Joachim P. Spatz,et al.  Micellar Inorganic–Polymer Hybrid Systems—A Tool for Nanolithography , 1999 .

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

[132]  W. G. Characklis Bioengineering report: Fouling biofilm development: A process analysis , 1981 .

[133]  G. Whitesides,et al.  Soft lithography in biology and biochemistry. , 2001, Annual review of biomedical engineering.

[134]  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.

[135]  J. Lannutti,et al.  Nanotopographic control of cytoskeletal organization. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[136]  Katsuhiko Ariga,et al.  Immobilization of biomaterials to nano-assembled films (self-assembled monolayers, Langmuir-Blodgett films, and layer-by-layer assemblies) and their related functions. , 2006, Journal of nanoscience and nanotechnology.

[137]  L. Wick,et al.  Influence of the Surface Topography of Stainless Steel on Bacterial Adhesion , 2002 .

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

[139]  M. Ginsberg,et al.  Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. , 1991, Trends in biochemical sciences.

[140]  Wei Zhou,et al.  The anatase phase of nanotopography titania plays an important role on osteoblast cell morphology and proliferation , 2008, Journal of materials science. Materials in medicine.

[141]  Y. L. Jeyachandran,et al.  Bacterial adhesion studies on titanium, titanium nitride and modified hydroxyapatite thin films , 2007 .

[142]  A S G Curtis,et al.  Morphological and microarray analysis of human fibroblasts cultured on nanocolumns produced by colloidal lithography. , 2005, European cells & materials.

[143]  S. Baldelli,et al.  Sum frequency generation microscopy of microcontact-printed mixed self-assembled monolayers. , 2006, The journal of physical chemistry. B.

[144]  D. Ingber,et al.  Mechanotransduction: All Signals Point to Cytoskeleton, Matrix, and Integrins , 2002, Science's STKE.

[145]  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.

[146]  T. Webster,et al.  The impact of diamond nanocrystallinity on osteoblast functions. , 2009, Biomaterials.

[147]  G. Camussi,et al.  Endothelization and adherence of leucocytes to nanostructured surfaces. , 2003, Biomaterials.

[148]  Christian Eggeling,et al.  Macromolecular-scale resolution in biological fluorescence microscopy. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[149]  J. Costerton,et al.  Introduction to biofilm. , 1999, International journal of antimicrobial agents.

[150]  Matthew John Dalby,et al.  Changes in fibroblast morphology in response to nano-columns produced by colloidal lithography. , 2004, Biomaterials.

[151]  R Geoff Richards,et al.  Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. , 2009, Journal of biomedical materials research. Part A.

[152]  S. Pan,et al.  Vitamin E TPGS-emulsified poly(lactic-co-glycolic acid) nanoparticles for cardiovascular restenosis treatment. , 2007, Nanomedicine.

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

[154]  Thomas J Webster,et al.  The role of nanometer and sub-micron surface features on vascular and bone cell adhesion on titanium. , 2008, Biomaterials.

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

[156]  F. Kienberger,et al.  A new, simple method for linking of antibodies to atomic force microscopy tips. , 2007, Bioconjugate chemistry.

[157]  R. G. Richards,et al.  Focal adhesion interactions with topographical structures: a novel method for immuno‐SEM labelling of focal adhesions in S‐phase cells , 2008, Journal of microscopy.

[158]  Hywel Morgan,et al.  Superhydrophobicity and superhydrophilicity of regular nanopatterns. , 2005, Nano letters.

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

[160]  Joshua R Porter,et al.  Biodegradable poly(epsilon-caprolactone) nanowires for bone tissue engineering applications. , 2009, Biomaterials.

[161]  M. Ferrari,et al.  Modulating cellular adhesion through nanotopography. , 2010, Biomaterials.

[162]  Hsuan-Liang Liu,et al.  Fibronectin modulates the morphology of osteoblast-like cells (MG-63) on nano-grooved substrates , 2009, Journal of materials science. Materials in medicine.

[163]  Nikolaj Gadegaard,et al.  The response of fibroblasts to hexagonal nanotopography fabricated by electron beam lithography. , 2008, Journal of biomedical materials research. Part A.

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

[165]  Benjamin Geiger,et al.  Cell interactions with hierarchically structured nano-patterned adhesive surfaces. , 2009, Soft matter.

[166]  H. C. van der Mei,et al.  Influence of wear and overwear on surface properties of etafilcon A contact lenses and adhesion of Pseudomonas aeruginosa. , 2002, Investigative ophthalmology & visual science.

[167]  Hung-Ta Wang,et al.  The control of cell adhesion and viability by zinc oxide nanorods. , 2008, Biomaterials.

[168]  J. Rossier,et al.  Integrating whole transcriptome assays on a lab-on-a-chip for single cell gene profiling. , 2008, Lab on a chip.

[169]  O. Soppera,et al.  Opposite responses of cells and bacteria to micro/nanopatterned surfaces prepared by pulsed plasma polymerization and UV-irradiation. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[170]  Bharat Bhushan,et al.  Nanoscale adhesion, friction and wear studies of biomolecules on silicon based surfaces. , 2006, Acta biomaterialia.

[171]  Nikolaj Gadegaard,et al.  Osteoprogenitor response to low-adhesion nanotopographies originally fabricated by electron beam lithography , 2007, Journal of materials science. Materials in medicine.

[172]  C. Siedlecki,et al.  Submicron poly(L-lactic acid) pillars affect fibroblast adhesion and proliferation. , 2007, Journal of biomedical materials research. Part A.

[173]  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.

[174]  M. Koizumi,et al.  Development of a high lateral resolution TOF-SIMS apparatus for single particle analysis , 2008 .

[175]  Joanna Verran,et al.  Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. , 2005, Colloids and surfaces. B, Biointerfaces.

[176]  N. Gadegaard,et al.  3D polymer scaffolds for tissue engineering. , 2006, Nanomedicine.

[177]  Brendon M. Baker,et al.  New directions in nanofibrous scaffolds for soft tissue engineering and regeneration , 2009, Expert review of medical devices.

[178]  H. Imai,et al.  Adhesion of osteoblast-like cells on nanostructured hydroxyapatite. , 2010, Acta biomaterialia.

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

[180]  A. Curtis,et al.  Nonadhesive nanotopography: fibroblast response to poly(n-butyl methacrylate)-poly(styrene) demixed surface features. , 2003, Journal of biomedical materials research. Part A.

[181]  Maxence Bigerelle,et al.  Roughness characteristic length scales of micro-machined surfaces: A multi-scale modelling , 2007 .

[182]  S. Coskun,et al.  Whole genome amplification from a single cell: a new era for preimplantation genetic diagnosis , 2007, Prenatal diagnosis.

[183]  Tim H. Taminiau,et al.  λ/4 Resonance of an Optical Monopole Antenna Probed by Single Molecule Fluorescence , 2007 .

[184]  P. Milani,et al.  Biocompatibility of cluster-assembled nanostructured TiO2 with primary and cancer cells. , 2006, Biomaterials.

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

[186]  M. Dalby,et al.  The effect of the RACK1 signalling protein on the regulation of cell adhesion and cell contact guidance on nanometric grooves. , 2008, Biomaterials.

[187]  Matthew J Dalby,et al.  The fibroblast response to tubes exhibiting internal nanotopography. , 2005, Biomaterials.

[188]  A. Curtis,et al.  Tubes with Controllable Internal Nanotopography , 2004 .

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

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

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

[192]  M. Fletcher,et al.  Effects of substratum wettability and molecular topography on the initial adhesion of bacteria to chemically defined substrata a b , 1997 .

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

[194]  Lydie Ploux,et al.  Bacteria/Material Interfaces: Role of the Material and Cell Wall Properties , 2010 .

[195]  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.

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

[197]  K. Whitehead,et al.  The effect of surface topography on the retention of microorganisms , 2006 .

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

[199]  J. Jansen,et al.  Scanning electron microscopic, transmission electron microscopic, and confocal laser scanning microscopic observation of fibroblasts cultured on microgrooved surfaces of bulk titanium substrata. , 1998, Journal of biomedical materials research.

[200]  C. D. W. Wilkinson,et al.  The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading , 2007, Journal of materials science. Materials in medicine.

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

[202]  David J. Whitehouse,et al.  Handbook of Surface Metrology , 2023 .

[203]  Marcus Textor,et al.  An inverted microcontact printing method on topographically structured polystyrene chips for arrayed micro-3-D culturing of single cells. , 2005, Biomaterials.

[204]  V. Truskett,et al.  Trends in imprint lithography for biological applications. , 2006, Trends in biotechnology.

[205]  Christopher Cannizzaro,et al.  Nanofabrication and microfabrication of functional materials for tissue engineering. , 2007, Tissue engineering.

[206]  F. L. Yap,et al.  Protein and cell micropatterning and its integration with micro/nanoparticles assembly. , 2007, Biosensors & bioelectronics.

[207]  G. Leggett,et al.  Influence of solvent environment and tip chemistry on the contact mechanics of tip-sample interactions in friction force microscopy of self-assembled monolayers of mercaptoundecanoic Acid and dodecanethiol. , 2007, Langmuir : the ACS journal of surfaces and colloids.

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

[209]  Matthew J Dalby,et al.  Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. , 2002, Experimental cell research.

[210]  Kazuki Kurimoto,et al.  Global single-cell cDNA amplification to provide a template for representative high-density oligonucleotide microarray analysis , 2007, Nature Protocols.

[211]  Y. L. Jeyachandran,et al.  A study on bacterial attachment on titanium and hydroxyapatite based films , 2006 .

[212]  Christopher J Murphy,et al.  The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. , 2006, Biomaterials.

[213]  Urs P. Wild,et al.  Fabricating arrays of single protein molecules on glass using microcontact printing , 2003 .

[214]  D. McClay The role of thin filopodia in motility and morphogenesis. , 1999, Experimental cell research.

[215]  B. Logan,et al.  Probing Bacterial Electrosteric Interactions Using Atomic Force Microscopy , 2000 .

[216]  Patrik Schmuki,et al.  TiO2 nanotube surfaces: 15 nm--an optimal length scale of surface topography for cell adhesion and differentiation. , 2009, Small.

[217]  A multi-scale approach of roughness measurements: Evaluation of the relevant scale , 2007 .

[218]  H. C. van der Mei,et al.  Multiple linear regression analysis of bacterial deposition to polyurethane coatings after conditioning film formation in the marine environment. , 2004, Microbiology.

[219]  Antonio Nanci,et al.  Surface Nanopatterning to Control Cell Growth , 2008 .

[220]  Robert Langer,et al.  A biodegradable and biocompatible gecko-inspired tissue adhesive , 2008, Proceedings of the National Academy of Sciences.

[221]  A. Becker,et al.  Systems nanobiology: from quantitative single molecule biophysics to microfluidic-based single cell analysis. , 2007, Sub-cellular biochemistry.

[222]  S. Hanks,et al.  Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. , 2006, Biophysical journal.

[223]  C. Prigent-Combaret,et al.  Abiotic Surface Sensing and Biofilm-Dependent Regulation of Gene Expression in Escherichia coli , 1999, Journal of bacteriology.

[224]  Tae Gwan Park,et al.  Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly(D,L-lactic-co-glycolic acid) nanofiber mesh. , 2006, Tissue engineering.

[225]  Peter Gasteier,et al.  Nanostructured Ordering of Fluorescent Markers and Single Proteins on Substrates , 2005, Chembiochem : a European journal of chemical biology.