A practical review on the measurement tools for cellular adhesion force

Cell-cell and cell-matrix adhesions are fundamental in all multicellular organisms. They play a key role in cellular growth, differentiation, pattern formation and migration. Cell-cell adhesion is substantial in the immune response, pathogen-host interactions, and tumor development. The success of tissue engineering and stem cell implantations strongly depends on the fine control of live cell adhesion on the surface of natural or biomimetic scaffolds. Therefore, the quantitative and precise measurement of the adhesion strength of living cells is critical, not only in basic research but in modern technologies, too. Several techniques have been developed or are under development to quantify cell adhesion. All of them have their pros and cons, which has to be carefully considered before the experiments and interpretation of the recorded data. Current review provides a guide to choose the appropriate technique to answer a specific biological question or to complete a biomedical test by measuring cell adhesion.

[1]  R. Rand,et al.  MECHANICAL PROPERTIES OF THE RED CELL MEMBRANE. II. VISCOELASTIC BREAKDOWN OF THE MEMBRANE. , 1964, Biophysical journal.

[2]  C F Quate,et al.  Imaging crystals, polymers, and processes in water with the atomic force microscope. , 1989, Science.

[3]  G. Wessel,et al.  Intercellular recognition: quantitation of initial binding events. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[4]  G. Georgiou,et al.  Molecular determinants of bacterial adhesion monitored by atomic force microscopy. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Ben Fabry,et al.  Three-dimensional force microscopy of cells in biopolymer networks , 2015, Nature Methods.

[6]  Yves F Dufrêne,et al.  Single-cell force spectroscopy of the medically important Staphylococcus epidermidis-Candida albicans interaction. , 2013, Nanoscale.

[7]  U. S. Schwarz,et al.  Coupling biochemistry and mechanics in cell adhesion: a model for inhomogeneous stress fiber contraction , 2007, 0707.2551.

[8]  Rahul Roy,et al.  A practical guide to single-molecule FRET , 2008, Nature Methods.

[9]  S Chien,et al.  Determination of junction avidity of cytolytic T cell and target cell. , 1986, Science.

[10]  Clare M Waterman,et al.  High resolution traction force microscopy based on experimental and computational advances. , 2008, Biophysical journal.

[11]  Tomaso Zambelli,et al.  Template‐Free 3D Microprinting of Metals Using a Force‐Controlled Nanopipette for Layer‐by‐Layer Electrodeposition , 2016, Advanced materials.

[12]  Jin-Yu Shao,et al.  A modified micropipette aspiration technique and its application to tether formation from human neutrophils. , 2002, Journal of biomechanical engineering.

[13]  David G. Grier,et al.  Evolution of a colloidal critical state in an optical pinning potential landscape , 2002 .

[14]  W. Saxinger,et al.  A simple method for measurement of cell-substrate attachment forces: application to HIV-1 Tat. , 1997, Journal of cell science.

[15]  Kevin T. Turner,et al.  Methods to Measure the Strength of Cell Adhesion to Substrates , 2010 .

[16]  Flemming Besenbacher,et al.  QCM-D studies of attachment and differential spreading of pre-osteoblastic cells on Ta and Cr surfaces. , 2006, Biomaterials.

[17]  Henny C van der Mei,et al.  Inhibition of adhesion of yeasts and bacteria by poly(ethylene oxide)-brushes on glass in a parallel plate flow chamber. , 2003, Microbiology.

[18]  Ching-Wei Chang,et al.  Vinculin tension distributions of individual stress fibers within cell–matrix adhesions , 2013, Journal of Cell Science.

[19]  Marcus Textor,et al.  Poly(l-lysine)-g-poly(ethylene glycol) Layers on Metal Oxide Surfaces: Surface-Analytical Characterization and Resistance to Serum and Fibrinogen Adsorption , 2001 .

[20]  Marcus Textor,et al.  Ligand-Specific Targeting of Microspheres to Phagocytes by Surface Modification with Poly(L-Lysine)-Grafted Poly(Ethylene Glycol) Conjugate , 2003, Pharmaceutical Research.

[21]  Nathan D. Gallant,et al.  Micropatterned surfaces to engineer focal adhesions for analysis of cell adhesion strengthening , 2002 .

[22]  Jens Friedrichs,et al.  Revealing Early Steps of α2β1 Integrin-mediated Adhesion to Collagen Type I by Using Single-Cell Force Spectroscopy , 2007 .

[23]  Harold P. Erickson,et al.  Force Measurements of the α5β1 Integrin–Fibronectin Interaction , 2003 .

[24]  David Alsteens,et al.  Atomic force microscopy-based characterization and design of biointerfaces , 2017 .

[25]  Xinzeng Feng,et al.  Toward single cell traction microscopy within 3D collagen matrices. , 2013, Experimental cell research.

[26]  A. Goldstein,et al.  Effect of adsorbed fibronectin concentration on cell adhesion and deformation under shear on hydrophobic surfaces. , 2002, Journal of biomedical materials research.

[27]  A S Rudolph,et al.  Cellular and cytoskeleton morphology and strength of adhesion of cells on self-assembled monolayers of organosilanes. , 1998, Experimental cell research.

[28]  Michael Sheetz,et al.  Integrin and cadherin clusters: A robust way to organize adhesions for cell mechanics , 2017, BioEssays : news and reviews in molecular, cellular and developmental biology.

[29]  E O Pettersen,et al.  Cell adhesion force microscopy. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  David J Mooney,et al.  Quantifying the relation between adhesion ligand–receptor bond formation and cell phenotype , 2006, Proceedings of the National Academy of Sciences.

[31]  H C van der Mei,et al.  Influence of substratum wettability on the strength of adhesion of human fibroblasts. , 1992, Biomaterials.

[32]  Shu Chien,et al.  Live Cells Exert 3-Dimensional Traction Forces on Their Substrata , 2009, Cellular and molecular bioengineering.

[33]  Christian Oddou,et al.  A cellular tensegrity model to analyse the structural viscoelasticity of the cytoskeleton. , 2002, Journal of theoretical biology.

[34]  Csaba Hős,et al.  Single Cell Adhesion Assay Using Computer Controlled Micropipette , 2014, PloS one.

[35]  H Kaltner,et al.  Differences in zero-force and force-driven kinetics of ligand dissociation from beta-galactoside-specific proteins (plant and animal lectins, immunoglobulin G) monitored by plasmon resonance and dynamic single molecule force microscopy. , 2000, Archives of biochemistry and biophysics.

[36]  Steven M. Block,et al.  Force and velocity measured for single kinesin molecules , 1994, Cell.

[37]  Daniel J Müller,et al.  Imaging and manipulation of biological structures with the AFM. , 2002, Micron.

[38]  Kristyn S Masters,et al.  Measurement of single-cell adhesion strength using a microfluidic assay , 2010, Biomedical microdevices.

[39]  Yang Liu,et al.  Three-Dimensional Nanoprinting via Direct Delivery. , 2017, The journal of physical chemistry. B.

[40]  L. Stryer,et al.  Energy transfer: a spectroscopic ruler. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Wilkinson,et al.  A parallel-plate flow chamber to study initial cell adhesion on a nanofeatured surface , 2004, IEEE Transactions on NanoBioscience.

[42]  Robert Horvath,et al.  Bacteria repellent layer made of flagellin , 2018 .

[43]  B. Ladoux,et al.  Physically based principles of cell adhesion mechanosensitivity in tissues , 2012, Reports on progress in physics. Physical Society.

[44]  K. Marx,et al.  A quartz crystal microbalance cell biosensor: detection of microtubule alterations in living cells at nM nocodazole concentrations. , 2001, Biosensors & bioelectronics.

[45]  Marcus Textor,et al.  Influence of PEG architecture on protein adsorption and conformation. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[46]  R. Messer,et al.  Attachment of human epithelial cells and periodontal ligament fibroblasts to tooth dentin. , 2006, Journal of biomedical materials research. Part A.

[47]  K Bergman,et al.  Characterization of photodamage to Escherichia coli in optical traps. , 1999, Biophysical journal.

[48]  Anne Simmons,et al.  Monitoring cell adhesion on tantalum and oxidised polystyrene using a quartz crystal microbalance with dissipation. , 2006, Biomaterials.

[49]  W. Nelson,et al.  Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell–cell adhesion , 2007, The Journal of cell biology.

[50]  P Ducheyne,et al.  Quantification of cell adhesion using a spinning disc device and application to surface-reactive materials. , 1997, Biomaterials.

[51]  Benjamin Geiger,et al.  Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption , 2003, Journal of Cell Science.

[52]  J. Feder,et al.  Characteristic protein adhesion forces on glass and polystyrene substrates by atomic force microscopy , 1998 .

[53]  A. Goldstein,et al.  Application of fluid mechanic and kinetic models to characterize mammalian cell detachment in a radial-flow chamber. , 1997, Biotechnology and bioengineering.

[54]  Catherine D Reyes,et al.  A centrifugation cell adhesion assay for high-throughput screening of biomaterial surfaces. , 2003, Journal of biomedical materials research. Part A.

[55]  R. Merkel,et al.  Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy , 1999, Nature.

[56]  T. Beveridge,et al.  Bacterial Recognition of Mineral Surfaces: Nanoscale Interactions Between Shewanella and α-FeOOH , 2001, Science.

[57]  K. Neuman,et al.  Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy , 2008, Nature Methods.

[58]  E. Evans,et al.  Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. , 1999, Biophysical chemistry.

[59]  Jeremy J. Ramsden,et al.  Dependence of cancer cell adhesion kinetics on integrin ligand surface density measured by a high-throughput label-free resonant waveguide grating biosensor , 2014, Scientific Reports.

[60]  Jeen-Shang Lin,et al.  Determining substrate displacement and cell traction fields--a new approach. , 2006, Journal of theoretical biology.

[61]  G. Truskey,et al.  Relationship between 3T3 cell spreading and the strength of adhesion on glass and silane surfaces. , 1993, Biomaterials.

[62]  Gerhard Wagner,et al.  TCR Mechanobiology: Torques and Tunable Structures Linked to Early T Cell Signaling , 2012, Front. Immun..

[63]  David Boettiger,et al.  BCR-ABL-induced adhesion defects are tyrosine kinase-independent. , 2002, Blood.

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

[65]  Robert Horvath,et al.  Green tea polyphenol tailors cell adhesivity of RGD displaying surfaces: multicomponent models monitored optically , 2017, Scientific Reports.

[66]  Xiong Wang,et al.  Studies on single-cell adhesion probability between lymphocytes and endothelial cells with micropipette technique. , 2002, Microvascular research.

[67]  Gaudenz Danuser,et al.  Mechanical Feedback through E-Cadherin Promotes Direction Sensing during Collective Cell Migration , 2014, Cell.

[68]  Ryosuke Ogaki,et al.  Temperature-induced ultradense PEG polyelectrolyte surface grafting provides effective long-term bioresistance against mammalian cells, serum, and whole blood. , 2012, Biomacromolecules.

[69]  C. Siegerist,et al.  Reproducible Imaging and Dissection of Plasmid DNA Under Liquid with the Atomic Force Microscope , 1992, Science.

[70]  Thomas Gervais,et al.  Flow-induced deformation of shallow microfluidic channels. , 2006, Lab on a chip.

[71]  G. J. Verkerke,et al.  Comparison of Velocity Profiles for Different Flow Chamber Designs Used in Studies of Microbial Adhesion to Surfaces , 2003, Applied and Environmental Microbiology.

[72]  E. Evans Probing the relation between force--lifetime--and chemistry in single molecular bonds. , 2001, Annual review of biophysics and biomolecular structure.

[73]  Kishan Dholakia,et al.  Optical micromanipulation takes hold , 2006, SPIE Optics + Photonics.

[74]  J. Wang,et al.  Spatial patterning of cell proliferation and differentiation depends on mechanical stress magnitude. , 2009, Journal of biomechanics.

[75]  S. Albelda,et al.  Role of integrins and other cell adhesion molecules in tumor progression and metastasis. , 1993, Laboratory investigation; a journal of technical methods and pathology.

[76]  P. Lin,et al.  Endothelial cell adhesion molecules and cancer progression. , 2007, Current medicinal chemistry.

[77]  Robert Horvath,et al.  Imageless microscopy of surface patterns using optical waveguides , 2008 .

[78]  Tomaso Zambelli,et al.  Bacterial adhesion force quantification by fluidic force microscopy. , 2015, Nanoscale.

[79]  Robert Horvath,et al.  Optical anisotropy of flagellin layers: in situ and label-free measurement of adsorbed protein orientation using OWLS. , 2013, Analytical chemistry.

[80]  Robert Horvath,et al.  High-Resolution Adhesion Kinetics of EGCG-Exposed Tumor Cells on Biomimetic Interfaces: Comparative Monitoring of Cell Viability Using Label-Free Biosensor and Classic End-Point Assays , 2018, ACS omega.

[81]  Peng Guo,et al.  Quantifying cell-adhesion strength with micropipette manipulation: principle and application. , 2004, Frontiers in bioscience : a journal and virtual library.

[82]  J. Mitchison,et al.  The Mechanical Properties of the Cell Surface , 1955 .

[83]  R. Horváth,et al.  Optical biosensors for cell adhesion , 2009, Journal of receptor and signal transduction research.

[84]  Hermann E. Gaub,et al.  Measuring Cell Adhesion Forces with the Atomic Force Microscope at the Molecular Level , 2002, Cells Tissues Organs.

[85]  R. Marchant,et al.  Force measurements on platelet surfaces with high spatial resolution under physiological conditions. , 2000, Colloids and surfaces. B, Biointerfaces.

[86]  B. Geiger,et al.  Transmembrane crosstalk between the extracellular matrix--cytoskeleton crosstalk. , 2001, Nature reviews. Molecular cell biology.

[87]  L. Stryer Fluorescence energy transfer as a spectroscopic ruler. , 1978, Annual review of biochemistry.

[88]  S. Roseman,et al.  A quantitative assay for intercellular adhesion. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Edin Sarajlic,et al.  Force-controlled spatial manipulation of viable mammalian cells and micro-organisms by means of FluidFM technology , 2010 .

[90]  Jens Friedrichs,et al.  Stimulated single‐cell force spectroscopy to quantify cell adhesion receptor crosstalk , 2010, Proteomics.

[91]  N. Balaban,et al.  Calculation of forces at focal adhesions from elastic substrate data: the effect of localized force and the need for regularization. , 2002, Biophysical journal.

[92]  E. Evans,et al.  Dynamic strength of molecular adhesion bonds. , 1997, Biophysical journal.

[93]  J. Mitchison,et al.  The Mechanical Properties of the Cell Surface I. The Cell Elastimeter , 1954 .

[94]  David J Mooney,et al.  Fluorescent resonance energy transfer: A tool for probing molecular cell-biomaterial interactions in three dimensions. , 2007, Biomaterials.

[95]  Matthew C. Dixon,et al.  Quartz crystal microbalance with dissipation monitoring: enabling real-time characterization of biological materials and their interactions. , 2008, Journal of biomolecular techniques : JBT.

[96]  O. Thoumine,et al.  Comparison of the mechanical properties of normal and transformed fibroblasts. , 1997, Biorheology.

[97]  J. Weisel,et al.  Binding strength and activation state of single fibrinogen-integrin pairs on living cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[98]  Z. Shao,et al.  Atomic force microscopy of cholera toxin B-oligomers bound to bilayers of biologically relevant lipids. , 1995, Journal of molecular biology.

[99]  D E Leckband,et al.  Cadherin adhesion and mechanotransduction. , 2014, Annual review of cell and developmental biology.

[100]  Xavier Trepat,et al.  Quantifying forces in cell biology , 2017, Nature Cell Biology.

[101]  S. Hubchak,et al.  P(AAm-co-EG) Interpenetrating Polymer Networks Grafted to Oxide Surfaces: Surface Characterization, Protein Adsorption, and Cell Detachment Studies , 1997 .

[102]  D. Boettiger,et al.  Force required to break alpha5beta1 integrin-fibronectin bonds in intact adherent cells is sensitive to integrin activation state. , 1998, The Journal of biological chemistry.

[103]  Jean-Michel Piau,et al.  Single-cell adhesion probed in-situ using optical tweezers: a case study with Saccharomyces cerevisiae , 2012 .

[104]  Jean-Michel Piau,et al.  The initial single yeast cell adhesion on glass via optical trapping and Derjaguin-Landau-Verwey-Overbeek predictions. , 2008, The Journal of chemical physics.

[105]  Alan Rick Horwitz,et al.  Actin-Based Adhesion Modules Mediate Cell Interactions with the Extracellular Matrix and Neighboring Cells. , 2017, Cold Spring Harbor perspectives in biology.

[106]  Gerber,et al.  Atomic force microscope. , 1986, Physical review letters.

[107]  A. Dunn,et al.  Molecular tension sensors report forces generated by single integrin molecules in living cells. , 2013, Nano letters.

[108]  G Büldt,et al.  Force-induced conformational change of bacteriorhodopsin. , 1995, Journal of molecular biology.

[109]  Driss Mazouzi,et al.  AFM and FluidFM Technologies: Recent Applications in Molecular and Cellular Biology , 2018, Scanning.

[110]  Bálint Szabó,et al.  Complement MASP-1 enhances adhesion between endothelial cells and neutrophils by up-regulating E-selectin expression. , 2016, Molecular immunology.

[111]  K. Salaita,et al.  Lighting Up the Force: Investigating Mechanisms of Mechanotransduction Using Fluorescent Tension Probes , 2015, Molecular and Cellular Biology.

[112]  Amelia Ahmad Khalili,et al.  A Review of Cell Adhesion Studies for Biomedical and Biological Applications , 2015, International journal of molecular sciences.

[113]  A C BURTON,et al.  MECHANICAL PROPERTIES OF THE RED CELL MEMBRANE. I. MEMBRANE STIFFNESS AND INTRACELLULAR PRESSURE. , 1964, Biophysical journal.

[114]  David Boettiger,et al.  A novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397. , 2003, Molecular biology of the cell.

[115]  Zhaochun Yang,et al.  Validation of the Boussinesq equation for use in traction field determination , 2011, Computer methods in biomechanics and biomedical engineering.

[116]  A. Engel,et al.  Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. , 1999, Journal of molecular biology.

[117]  Robert Horvath,et al.  Biomimetic Dextran-Based Hydrogel Layers for Cell Micropatterning over Large Areas Using the FluidFM BOT Technology. , 2019, Langmuir : the ACS journal of surfaces and colloids.

[118]  M A Horton,et al.  Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy. , 1999, Biochemical and biophysical research communications.

[119]  R. Hochmuth,et al.  Micropipette aspiration of living cells. , 2000, Journal of biomechanics.

[120]  Shai Shaham,et al.  FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis , 2015, eLife.

[121]  H C van der Mei,et al.  Fluid shear induced endothelial cell detachment from glass--influence of adhesion time and shear stress. , 1994, Medical Engineering and Physics.

[122]  R. Dobarzić,et al.  [Fluorescence microscopy]. , 1975, Plucne bolesti i tuberkuloza.

[123]  Wesley R. Legant,et al.  Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions , 2012, Proceedings of the National Academy of Sciences.

[124]  Daniel J. Muller,et al.  A new technical approach to quantify cell-cell adhesion forces by AFM. , 2006, Ultramicroscopy.

[125]  Robert Horvath,et al.  In-situ and label-free optical monitoring of the adhesion and spreading of primary monocytes isolated from human blood: dependence on serum concentration levels. , 2014, Biosensors & bioelectronics.

[126]  Evan Evans,et al.  Five challenges to bringing single-molecule force spectroscopy into living cells , 2011, Nature Methods.

[127]  Kenneth M. Yamada,et al.  Transmembrane crosstalk between the extracellular matrix and the cytoskeleton , 2001, Nature Reviews Molecular Cell Biology.

[128]  Hermann E. Gaub,et al.  Discrete interactions in cell adhesion measured by single-molecule force spectroscopy , 2000, Nature Cell Biology.

[129]  A. Goldstein,et al.  Examination of membrane rupture as a mechanism for mammalian cell detachment from fibronectin-coated biomaterials. , 2003, Journal of biomedical materials research. Part A.

[130]  R. Fässler,et al.  Integrin-mediated mechanotransduction , 2016, The Journal of cell biology.

[131]  R. Lovitt,et al.  The measurement of Bacillus mycoides spore adhesion using atomic force microscopy, simple counting methods, and a spinning disk technique , 2002, Biotechnology and bioengineering.

[132]  Tomaso Zambelli,et al.  Rapid and Serial Quantification of Adhesion Forces of Yeast and Mammalian Cells , 2012, PloS one.

[133]  Carsten Grashoff,et al.  Investigating piconewton forces in cells by FRET-based molecular force microscopy. , 2017, Journal of structural biology.

[134]  Stephanus Büttgenbach,et al.  Polyelectrolyte multilayer surface functionalization of poly(dimethylsiloxane) (PDMS) for reduction of yeast cell adhesion in microfluidic devices. , 2010, Biomicrofluidics.

[135]  David A Calderwood,et al.  Regulation of integrin-mediated adhesions. , 2015, Current opinion in cell biology.

[136]  H. Gaub,et al.  Intermolecular forces and energies between ligands and receptors. , 1994, Science.

[137]  Lee,et al.  The Effect of Fluid Shear Stress on Endothelial Cell Adhesiveness to Polymer Surfaces with Wettability Gradient. , 2000, Journal of colloid and interface science.

[138]  Maryam Tabrizian,et al.  Probing surface adhesion forces of Enterococcus faecalis to medical-grade polymers using atomic force microscopy. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[139]  Douglas A Lauffenburger,et al.  Microfluidic shear devices for quantitative analysis of cell adhesion. , 2004, Analytical chemistry.

[140]  Daniel J. Muller,et al.  Single-cell force spectroscopy , 2008, Journal of Cell Science.

[141]  Jean-Michel Piau,et al.  Removal forces and adhesion properties of Saccharomyces cerevisiae on glass substrates probed by optical tweezer. , 2007, The Journal of chemical physics.

[142]  J. Dai,et al.  Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. , 1995, Biophysical journal.

[143]  Taekjip Ha,et al.  Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics , 2010, Nature.

[144]  Paul A. DiMilla,et al.  Comparison of converging and diverging radial flow for measuring cell adhesion , 1998 .

[145]  Carsten Grashoff,et al.  How to Measure Molecular Forces in Cells: A Guide to Evaluating Genetically-Encoded FRET-Based Tension Sensors , 2014, Cellular and Molecular Bioengineering.

[146]  B. Tromberg,et al.  Cell damage in near-infrared multimode optical traps as a result of multiphoton absorption. , 1996, Optics letters.

[147]  C Bechinger,et al.  Imaging of cell/substrate contacts of living cells with surface plasmon resonance microscopy. , 1999, Biophysical journal.

[148]  Jeffrey J. Fredberg,et al.  Reinforcement versus Fluidization in Cytoskeletal Mechanoresponsiveness , 2009, PloS one.

[149]  Beth L. Pruitt,et al.  E-cadherin is under constitutive actomyosin-generated tension that is increased at cell–cell contacts upon externally applied stretch , 2012, Proceedings of the National Academy of Sciences.

[150]  S. Cooper,et al.  Physical property analysis and bacterial adhesion on a series of phosphonated polyurethanes. , 1997, Biomaterials.

[151]  Taekjip Ha,et al.  An Improved Surface Passivation Method for Single-Molecule Studies , 2014, Nature Methods.

[152]  Samuel Rosset,et al.  3-dimensional electrode patterning within a microfluidic channel using metal ion implantation. , 2010, Lab on a chip.

[153]  Robert Horvath,et al.  Automated single cell sorting and deposition in submicroliter drops , 2014 .

[154]  Robert Horvath,et al.  Kinetics and Structure of Self-Assembled Flagellin Monolayers on Hydrophobic Surfaces in the Presence of Hofmeister Salts: Experimental Measurement of the Protein Interfacial Tension at the Nanometer Scale , 2018, The Journal of Physical Chemistry C.

[155]  N. Gov Traction forces during collective cell motion , 2009, HFSP journal.

[156]  Robert Horvath,et al.  Flagellin based biomimetic coatings: From cell-repellent surfaces to highly adhesive coatings. , 2016, Acta biomaterialia.

[157]  Péter Fürjes,et al.  Automated single cell isolation from suspension with computer vision , 2016, Scientific Reports.

[158]  Feiya Li,et al.  Force measurements of the alpha5beta1 integrin-fibronectin interaction. , 2003, Biophysical journal.

[159]  O. Thoumine,et al.  Critical centrifugal forces induce adhesion rupture or structural reorganization in cultured cells. , 1996, Cell motility and the cytoskeleton.

[160]  Rafael Yuste,et al.  Fluorescence microscopy today , 2005, Nature Methods.

[161]  Douglas A Lauffenburger,et al.  Co-regulation of cell adhesion by nanoscale RGD organization and mechanical stimulus. , 2002, Journal of cell science.

[162]  Benoit Ladoux,et al.  Biophysics: Cells guided on their journey , 2009 .

[163]  T J Beveridge,et al.  Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and alpha-FeOOH. , 2001, Science.

[164]  S. Fisher,et al.  Quantifying the Strength of Bacterial Adhesive Interactions with Salivary Glycoproteins , 1995, Journal of dental research.

[165]  Tomaso Zambelli,et al.  FluidFM as a lithography tool in liquid: spatially controlled deposition of fluorescent nanoparticles. , 2013, Nanoscale.

[166]  Jens Friedrichs,et al.  Quantifying cellular adhesion to extracellular matrix components by single-cell force spectroscopy , 2010, Nature Protocols.

[167]  L. Weiss,et al.  The measurement of cell adhesion. , 1961, Experimental cell research.

[168]  D. McClay,et al.  Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response , 1989, The Journal of cell biology.

[169]  W Baumeister,et al.  Conformational change of the hexagonally packed intermediate layer of Deinococcus radiodurans monitored by atomic force microscopy , 1996, Journal of bacteriology.

[170]  Igor L. Medintz,et al.  Fluorescence resonance energy transfer between quantum dot donors and dye-labeled protein acceptors. , 2003, Journal of the American Chemical Society.

[171]  Christian Eggeling,et al.  Dissection of mechanical force in living cells by super-resolved traction force microscopy , 2017, Nature Protocols.

[172]  Evan Evans,et al.  Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[173]  R. Klebe,et al.  Isolation of a collagen-dependent cell attachment factor , 1974, Nature.

[174]  Daniel A. Hammer,et al.  Centrifugation assay of IgE‐mediated cell adhesion to antigen‐coated gels , 1994 .

[175]  R M Hochmuth,et al.  Micropipette suction for measuring piconewton forces of adhesion and tether formation from neutrophil membranes. , 1996, Biophysical journal.

[176]  Ulrich S Schwarz,et al.  Focal adhesions as mechanosensors: the two-spring model. , 2006, Bio Systems.

[177]  Eben Alsberg,et al.  FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[178]  Jeen-Shang Lin,et al.  Cell traction force and measurement methods , 2007, Biomechanics and modeling in mechanobiology.

[179]  Evan Evans,et al.  Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes , 2000 .

[180]  E. Evans,et al.  Strength of a weak bond connecting flexible polymer chains. , 1999, Biophysical journal.

[181]  Y. Dufrêne,et al.  Detection and localization of single molecular recognition events using atomic force microscopy , 2006, Nature Methods.

[182]  H. C. van der Mei,et al.  Development and use of a parallel-plate flow chamber for studying cellular adhesion to solid surfaces. , 1992, Journal of biomedical materials research.

[183]  A. Evans,et al.  A model for the contractility of the cytoskeleton including the effects of stress-fibre formation and dissociation , 2007, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[184]  L. Goldstein,et al.  Bead movement by single kinesin molecules studied with optical tweezers , 1990, Nature.

[185]  Eric Henderson,et al.  Atomic force microscopy and manipulation of living glial cells , 1993 .

[186]  W J Nelson,et al.  Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay , 1996, The Journal of cell biology.

[187]  R. Timpl,et al.  Substrate adhesion of rat hepatocytes: Mechanism of attachment to collagen substrates , 1981, Cell.

[188]  Kishan Dholakia,et al.  Optical micromanipulation takes hold , 2006 .

[189]  Chris J. Wright,et al.  Atomic Force Microscopy Study of the Adhesion of Saccharomyces cerevisiae. , 2001, Journal of colloid and interface science.

[190]  S Kaplanski,et al.  Granulocyte-endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow. , 1993, Biophysical journal.

[191]  Tomaso Zambelli,et al.  FluidFM: combining atomic force microscopy and nanofluidics in a universal liquid delivery system for single cell applications and beyond. , 2009, Nano letters.

[192]  S. Hénon,et al.  A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. , 1999, Biophysical journal.

[193]  David A. Weitz,et al.  Physical forces during collective cell migration , 2009 .

[194]  G Büldt,et al.  Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy. , 1995, Biophysical journal.

[195]  Robert Horvath,et al.  Adhesion kinetics of human primary monocytes, dendritic cells, and macrophages: Dynamic cell adhesion measurements with a label-free optical biosensor and their comparison with end-point assays. , 2016, Biointerphases.

[196]  M. Cybulsky,et al.  Getting to the site of inflammation: the leukocyte adhesion cascade updated , 2007, Nature Reviews Immunology.

[197]  Janos Vörös,et al.  RGD-grafted poly-L-lysine-graft-(polyethylene glycol) copolymers block non-specific protein adsorption while promoting cell adhesion. , 2003, Biotechnology and bioengineering.

[198]  E. Evans,et al.  Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. , 1995, Biophysical journal.

[199]  G Büldt,et al.  Immuno-atomic force microscopy of purple membrane. , 1996, Biophysical journal.

[200]  Bahman Anvari,et al.  Temporal effects of cell adhesion on mechanical characteristics of the single chondrocyte , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[201]  D. Ingber,et al.  Cellular tensegrity : defining new rules of biological design that govern the cytoskeleton , 2022 .

[202]  J. Lakowicz Principles of fluorescence spectroscopy , 1983 .

[203]  Mohammad Said Saidi,et al.  Biomechanical analysis of actin cytoskeleton function based on a spring network cell model , 2017 .

[204]  S. Weiss Fluorescence spectroscopy of single biomolecules. , 1999, Science.

[205]  L G Griffith,et al.  Cell adhesion and motility depend on nanoscale RGD clustering. , 2000, Journal of cell science.

[206]  Anna Erdei,et al.  CD11c/CD18 Dominates Adhesion of Human Monocytes, Macrophages and Dendritic Cells over CD11b/CD18 , 2016, PloS one.

[207]  Thorsten Hugel,et al.  The Study of Molecular Interactions by AFM Force Spectroscopy. , 2002 .

[208]  C. Simmons,et al.  Matrix-dependent adhesion of vascular and valvular endothelial cells in microfluidic channels. , 2007, Lab on a chip.

[209]  R. Waugh,et al.  Integrin Activation by Divalent Ions Affects Neutrophil Homotypic Adhesion , 2002, Annals of Biomedical Engineering.

[210]  W. Brownell,et al.  Membrane tether formation from outer hair cells with optical tweezers. , 2002, Biophysical journal.

[211]  Renzo Antolini,et al.  Optical micromanipulations inside yeast cells. , 2005, Applied optics.

[212]  B. Szabo,et al.  Cell sorting in a Petri dish controlled by computer vision , 2013, Scientific Reports.

[213]  J. Wang,et al.  Alpha-smooth muscle actin expression enhances cell traction force. , 2007, Cell motility and the cytoskeleton.

[214]  M C Miller,et al.  Expression of epithelial cell adhesion molecule in carcinoma cells present in blood and primary and metastatic tumors. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[215]  C. Quate,et al.  Forces in atomic force microscopy in air and water , 1989 .

[216]  Carsten Werner,et al.  A practical guide to quantify cell adhesion using single-cell force spectroscopy. , 2013, Methods.

[217]  Jean-Jacques Meister,et al.  Short-term binding of fibroblasts to fibronectin: optical tweezers experiments and probabilistic analysis , 2000, European Biophysics Journal.

[218]  Arthur E Johnson,et al.  Fluorescence Approaches for Determining Protein Conformations, Interactions and Mechanisms at Membranes , 2005, Traffic.

[219]  Steven P Gross,et al.  Application of optical traps in vivo. , 2003, Methods in enzymology.

[220]  Ming C. Wu,et al.  Massively parallel manipulation of single cells and microparticles using optical images , 2005, Nature.

[221]  Benjamin G Keselowsky,et al.  Quantitative methods for analysis of integrin binding and focal adhesion formation on biomaterial surfaces. , 2005, Biomaterials.

[222]  Roseanne M Ford,et al.  Characterizing the adhesion of motile and nonmotile Escherichia coli to a glass surface using a parallel-plate flow chamber. , 2002, Biotechnology and bioengineering.

[223]  Kuo-Kang Liu,et al.  Optical tweezers for single cells , 2008, Journal of The Royal Society Interface.

[224]  Tomaso Zambelli,et al.  Force-controlled manipulation of single cells: from AFM to FluidFM. , 2014, Trends in biotechnology.

[225]  D. Hammer,et al.  Influence of direction and type of applied force on the detachment of macromolecularly-bound particles from surfaces , 1996 .

[226]  Enrico Gratton,et al.  Fluid Shear Stress on Endothelial Cells Modulates Mechanical Tension across VE-Cadherin and PECAM-1 , 2013, Current Biology.

[227]  R. Waugh,et al.  Micromechanical tests of adhesion dynamics between neutrophils and immobilized ICAM-1. , 2004, Biophysical journal.

[228]  S Chien,et al.  Determination of adhesion force between single cell pairs generated by activated GpIIb-IIIa receptors. , 1993, Blood.

[229]  J. Wang,et al.  The principles and biological applications of cell traction force microscopy , 2010 .

[230]  D A Lauffenburger,et al.  Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength , 1993, The Journal of cell biology.

[231]  Fei Xu,et al.  NTA-Functionalized Poly(L-lysine)-g-Poly(Ethylene Glycol): A Polymeric Interface for Binding and Studying 6 His-tagged Proteins , 2005, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

[232]  Rolf Bos,et al.  Lateral and Perpendicular Interaction Forces Involved in Mobile and Immobile Adhesion of Microorganisms on Model Solid Surfaces , 1998, Current Microbiology.