SPM Investigation of Cells

It is hard to imagine a more fundamental as well as more complicated biological object than a living cell. In a short period of time the applications of AFM have been extended to such a complex field of biology as science of the cell [357, 959, 960, 961].

In this field Atomic Force Microscopy features not only high-resolution imaging of cellular structures below the optical limit, which is quite "natural" for this method, but also evaluation of the micromechanical properties of the cell and the ability to monitor cell dynamics and processes running in it even in real time. At present, no other microscopic techniques are able to provide directly both structural information of a biological sample and related functional information at such high spatial resolution [357]. Using AFM cells can be imaged directly requiring little or no sample pre-treatment and, what is quite importnat, in their most native physiological media such as aqueous solutions. Offering several advantages over conventional microscopic techniques AFM is successfully employed in combination with other methods such as electron microscopy, SNOM, PCT and others [981, 982, 983, 997, 998].

Direct imaging of fixed or living cells and subcellular structures provides important information on the architecture of the membrane, organelles and cytoskeleton of cells. AFM offers a unique opportunity to image, localize and identify integral membrane proteins at the surface of living cells [962, 963, 964, 965, 966, 967]. Although staining or fluorescent labeling to mark the proteins of interest can not be avoided due to the indiscriminative nature of AFM probing relative to chemical composition and nature of the objects, further improvements and extensions promise this problem to be solved. For instance, using a method proposed in [999], the functionality of membrane proteins such as ion channels can be identified using the Patch Clamp Technique (PCT) [980] and the density of the protein distribution over the membrane patch can also be estimated. This combination of AFM and PCT allows for lateral resolution of cytoskeletal elements from the patches as low as 10 nm [981]. To observe membrane structural features such as ruffles, lamellipodia, microspikes and microvilli, cell fixation is used [968, 969]. Because the plasma membrane prevents from observing the intracellular structure the means of its careful removal were developed [970].

Contact mode, commonly used in AFM, is not a very suitable mode for cell imaging since it affects the membrane in a destructive way. Therefore, tapping mode or intermittent contact AFM is preferable in such studies for high-resolution imaging of subcellular structures. The main problem that arises in this case is how to remove tje damping involved by the liquid environment and develop an appropriate contrast mechanism to improve quality [971, 972, 973, 974].

Another major AFM application in cell studies is real-time monitoring of living cells dynamics, intercellular interactions and response to internal and external perturbing factors [357, 975]. Examples include the exploration of exocytosis of a virus from an infected cell in real time [976], platelets shape transformation upon activation [977], cultured pancreas cells secreting the starch-digesting enzyme amylase [978].

The main problem in monitoring the dynamic behavior of the cell is minimizing the perturbation caused by the probe during the scanning process as well as maintaining stable environmental conditions for both temperature and pH value [357, 979]. Another technical challenge is achieving high temporal resolution since the time to acquire a full scan of a living cell often exceeds the characteristic alterations happening in it. Diminishing of undesirable cellular stimulation can be achieved by the implementation of the modified tapping mode technique in liquid or the development of a new technique in which much lower cantilever loading forces are required, and/or the design of novel AFM probes which are biochemically and mechanically compatible with biological samples [357]. The simplest remedy to increase temporal resolution is, obviously, to speed up the scan rate, often though at the expense of spatial resolution [984, 985, 986, 987]. Therefore, existing AFM apparatus and techniques allow to monitor certain dynamic cellular processes, such as cell growth, exocytotic and endocytotic events, which are not very fast in time and requires less power in spatial resolution, and to study the cell morphology in real time in the presence of growth factors, hormones, and other biological reagents. With the development of high scan rate AFM it may be possible to use AFM to monitor the processes that occur at the cell membrane during an antibody binding, vesicle transfer, channel blocking or gating, etc., and to obtain information on the delivery of a specific drug with molecular resolution [357].

Information about the micromechanical properties is quite important for cellular systems because it helps understanding cell architecture and its functions [975, 988, 989, 990, 991, 992, 993, 994]. Local elastic properties of a cell can be quantitatively derived from the force versus distance (F-S) curves obtained at fixed surface points using AFM. Cytosceleton is the main characteristic feature observed in AFM images and it is responsible for the mechanical properties of the cell. Cytosceleton generally defines the shape, activity and mobility of the cell. Data acquired from AFM measurements contains information about both topography and elasticity and these two types must be distinguished from each other. This can be done using the elasticity mapping technique. The accuracy of elasticity measurements depends upon a number of factors considered in [357]. Attention should be paid in the quantitative study of cell micromechanical properties [593, 988, 995].

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981 A scanning force microscopy for simultaneous force and patch-clamp measurements on living cell tissues
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959 Atomic force microscopy for high-resolution imaging in cell biology
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357 Atomic force microscopy imaging of living cells: progress, problems and prospects
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968 Atomic force microscopy of renal cells: Limits and prospects
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961 Biological applications of atomic force microscopy
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964 Cell-surface receptors and proteins on platelet membranes imaged by scanning force microscopy using immunogold contrast enhancement
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997 Combining optical and atomic force microscopy for life sciences research
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973 Deformation, contact time, and phase-contrast in tapping mode scanning force microscopy
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991 Differences in elasticity of vinculin-deficient F9 cells measured by magnetometry and atomic force microscopy
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994 Dynamic micromechanical properties of cultured rat atrial myocytes measured by atomic force microscopy
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977 Granular motion and membrane spreading during activation of human platelets imaged by atomic force microscopy
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999 Imaging excised apical plasma membrane patches of MDCK cells in physiological conditions with atomic force microscopy
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960 Imaging of living cells by atomic force microscopy
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987 Imaging ROMK1 inwardly rectifying ATP-sensitive K+ channel proteins using atomic force microscopy
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970 Imaging subcellular structures of rat mammary carcinoma cells by scanning force microscopy
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969 Imaging surface and submembranous structures with the atomic force microscope: A study on living cancer cells, fibroblasts and macrophages
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982 Imaging the internal and external pore structure of membranes in fluid: Tapping mode scanning ion conductance microscopy
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989 Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope
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974 Investigation of the image contrast of tapping-mode atomic force microscopy using protein-modified cantilever tips
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966 Localization of amiloride-sensitive sodium channels in A6 cells by atomic force microscopy
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962 Localization of individual calcium channels at the release face of a presynaptic nerve terminal
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593 Measuring elasticity of biological materials by atomic force microscopy
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995 Measuring the elastic properties of biological samples with the AFM
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993 Measuring the viscoelastic properties of human platelets with the atomic force microscope
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988 Mechanical and morphological properties of living 3T6 cells probed via scanning force microscopy
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998 Membrane deformation of living glial cells using atomic force microscopy
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986 Protein tracking and detection of protein motion using atomic force microscopy
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992 Relative microelastic mapping of living cells by atomic force microscopy
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984 Scan speed limit in atomic force microscopy
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983 Scanning ion conductance microscopy of living cells
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967 Structural changes in native membrane proteins monitored at subnanometer resolution with the atomic force microscopy: A review
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976 Structure and activation dynamics of RBL-2H3 cells observed with scanning force microscopy
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972 Studies of vibrating atomic force microscope cantilevers in liquid
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978 Surface dynamics in living acinar cells imaged by atomic force microscopy: Identification of plasma membrane structures involved in exocytosis
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963 Topography of the Leydig cell mitochondrial peripheral-type benzodiazepine receptor
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419 Atomic force microscopy to study direct neurite-mast cell (RBL) communication in vitro
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420 Atomic force microscopy to study the effects of ITIM-bearing FcgRIIB on the activation of RBL-2H3 cells
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470 Detection of the absorption of glucose molecules by living cells using atomic force microscopy
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474 Differences in F9 and 5.51 cell elasticity determined by cell poking and atomic force microscopy
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476 Direct observation of oxidative stress on the cell wall of Saccharomyces cerevisiae strains with atomic force microscopy
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495 Estimation for the elasticity of vascular endothelial cells on the basis of atomic force microscopy and Young's modulus of gelatin gels
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513 Glial cells with differential neurite growth-modulating properties probed by atomic force microscopy
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588 Measurement of morphological change in endothelial cells by osmotic pressure alteration under atomic force microscopy
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622 Morphological changes in living cell cultures following a-particle irradiation studied by optical and atomic force microscopy
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773 Three-dimensional characterization of interior structures of exocytotic apertures of nerve cells using atomic force microscopy
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795 Binding strength between cell adhesion proteoglycans measured by atomic force microscopy
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862 Investigation of the swelling of human skin cells in liquid media by tapping mode scanning force microscopy
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871 Local elastic properties of cells studied by SFM
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944 The effect of chitosan on stiffness and glycolytic activity of human bladder cells
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1044 Preparation of basal cell membranes for scanning probe microscopy
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1068 Studying the surface of soft materials (live cells) at high resolution by scanning probe microscopy: Challenges faced
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1080 Atomic force microscopy combined with confocal laser scanning microscopy: a new look at cells
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1531 In situ investigation of single living cells infected by viruses
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1535 Kinetics and mechanics of cell adhesion
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1329 New technologies in scanning probe microscopy for studying molecular interactions in cells
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1398 Use of AFM for imaging and measurement of the mechanical properties of light-convertible organelles in plants
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1399 Combination of AFM with an objective-type total internal reflection fluorescence microscope (TIRFM) for nanomanipulation of single cells
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1664 Surface morphological characterization of yeast cells by scanning force microscopy
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1665 Comparative study of the hydrophobicity of Candida parapsilosis 294 through macroscopic and microscopic analysis
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1700 Pushing, pulling, dragging, and vibrating renal epithelia by using atomic force microscopy
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1706 Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells
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1711 Determination of cellular strains by combined atomic force microscopy and finite element modeling
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1720 Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study
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1723 The assembly of amyloidogenic yeast sup35 as assessed by scanning (atomic) force microscopy: an analogy to linear colloidal aggregation?
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1726 Direct characterization of the physicochemical properties of fungal spores using functionalized AFM probes
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1729 Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation
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1731 Morphology and transverse stiffness of Drosophila myofibrils measured by atomic force microscopy
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1734 Direct probing by atomic force microscopy of the cell surface softness of a fibrillated and nonfibrillated oral streptococcal strain
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1747 Structure and dynamics of the fusion pores in live GH-secreting cells revealed using atomic force microscopy
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1752 An Atomic force microscopy investigation of bioadhesive polymer adsorption onto human buccal cells
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1753 The use of atomic force microscopy for the observation of corneal epithelium surface
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1756 Atomic force microscopy reveals two conformations of the 20 S proteasome from fission yeast
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1760 A comparative atomic force microscopy study on living skin fibroblasts and liver endothelial cells
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1769 Structural analysis of red blood cell membrane with an atomic force microscope
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1770 The cell biological application of carbon nanotube probes for atomic force microscopy: comparative studies of malaria-infected erythrocytes
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1771 Time-lapse viscoelastic imaging of living fibroblasts using force modulation mode in AFM
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1772 Observations of xenon gas-treated barley cells in solution by atomic force microscopy
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1790 Charting and unzipping the surface-layer of Corynebacterium glutamicum with the atomic force microscope
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1805 Combining constitutive materials modeling with atomic force microscopy to understand the mechanical properties of living cells
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2277 Membrane knobs of unfixed Plasmodium falciparum infected erythrocytes: new findings as revealed by atomic force microscopy and surface potential spectroscopy
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2041 Comparative scanning, transmission and atomic force microscopy of the microtubular cytoskeleton in fenestrated liver endothelial cells
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1880 Aldosterone activates the nuclear pore transporter in cultured kidney cells imaged with atomic force microscopy
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2040 Comparative atomic force and scanning electron microscopy: an investigation on fenestrated endothelial cells in vitro
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2390 Scanning force microscopy reveals ellipsoid shape of chicken erythrocyte nucleosomes
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1940 Atomic force microscopy of Escherichia coli FoF1-ATPase in reconstituted membranes
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1847 A non-invasive method for the tight anchoring of cells for scanning force microscopy
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1950 Atomic force microscopy of plant cell walls, plant cell wall polysaccharides and gels
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2003 Cellular and molecular mechanics by atomic force microscopy: capturing the exocytotic fusion pore in vivo?
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2263 Mapping cell wall polysaccharides of living microbial cells using atomic force microscopy
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2002 Cell viability and probe-cell membrane interactions of XR1 glial cells imaged by atomic force microscopy
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2413 Simultaneous imaging of the surface and the submembraneous cytoskeleton in living cells by tapping mode atomic force microscopy
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C. R. Acad. Sci. III, 320 (1997) 8, 637-643
2117 Electron probe X-ray microanalysis of cultured epithelial tumour cells with scanning electron microscopy
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1962 Atomic force microscopy studies of living cells: visualization of motility, division, aggregation, transformation, and apoptosis
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2100 Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells
F. Braet, R. De Zanger, E. Wisse
J. Microsc., 186 (1997) 1, 84-87
1955 Atomic force microscopy on living cells: aldosterone-induced localized cell swelling
S. W. Schneider, P. Pagel, J. Storck, Y. Yano, B. E. Sumpio, J. P. Geibel, H. Oberleithner
Kidney Blood Press Res., 21 (1998) 2-4, 256-258
2272 Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking
H. W. Wu, T. Kuhn, V. T. Moy
Scanning, 20 (1998) 5, 389-397
2241 Kinetic analysis of the mitotic cycle of living vertebrate cells by atomic force microscopy
J. A. Dvorak, E. Nagao
Exp. Cell. Res., 242 (1998) 1, 69-74
2110 Elastic properties of living fibroblasts as imaged using force modulation mode in atomic force microscopy
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Arch. Histol. Cytol., 61 (1998) 1, 57-63
1976 Atomic force microscopy: application to investigation of Escherichia coli morphology before and after exposure to cefodizime
P. C. Braga, D. Ricci
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2189 Imaging of the surface of living cells by low-force contact-mode atomic force microscopy
C. Le Grimellec, E. Lesniewska, M. C. Giocondi, E. Finot, V. Vie, J. P. Goudonnet
Biophys. J., 75 (1998) 2, 695-703
2440 Structure of the erythrocyte membrane skeleton as observed by atomic force microscopy
M. Takeuchi, H. Miyamoto, Y. Sako, H. Komizu, A. Kusumi
Biophys. J., 74 (1998) 5, 2171-2183
1927 Atomic force microscopy in effusion cytology
B. Ross, H. Motherby, F. Saurenbach, J. Frohn, M. Kube, A. Bocking
Anal. Quant. Cytol. Histol., 20 (1998) 2, 97-104
2112 Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy
M. Lekka, P. Laidler, D. Gil, J. Lekki, Z. Stachura, A. Z. Hrynkiewicz
European Biophysics Journal, 28 (1999) 4, 312-316
1971 Atomic force microscopy to study the degranulation in rat peritoneal mast cells after activation
R. Nakamura, M. Nakanishi
Immunology Letters, 69 (1999) 3, 307-310
2001 Cell adhesion force microscopy
G. Sagvolden, I. Giaever, E. O. Pettersen, J. Feder
Proc. Natl. Acad. Sci. USA, 96 (1999) 2, 471-476
2338 Phase imaging by atomic force microscopy: analysis of living homoiothermic vertebrate cells
E. Nagao, J. A. Dvorak
Biophys. J., 76 (1999) 6, 3289-3297
2051 Continuous detection of extracellular ATP on living cells by using atomic force microscopy
S. W. Schneider, M. E. Egan, B. P. Jena, W. B. Guggino, H. Oberleithner, J. P. Geibel
Proc. Natl. Acad. Sci. USA, 96 (1999) 21, 12180-12185
2185 Imaging of living cultured cells of an epithelial nature by atomic force microscopy
T. Ushiki, J. Hitomi, T. Umemoto, S. Yamamoto, H. Kanazawa, M. Shigeno
Arch. Histol. Cytol., 62 (1999) 1, 47-55
2403 Selective cleaning of the cell debris in human chromosome preparations studied by scanning force microscopy
J. Tamayo, M. Miles, A. Thein, P. Soothill
J. Struct. Biol., 128 (1999) 2, 200-210
2518 Topography of cell traces studied by atomic force microscopy
H. Zimmermann, R. Hagedorn, E. Richter, G. Fuhr
European Biophysics Journal, 28 (1999) 6, 516-525
2108 Effect of streptolysin O on the microelasticity of human platelets analyzed by atomic force microscopy
M. Walch, U. Ziegler, P. Groscurth
Ultramicroscopy, 82 (2000) 1-4, 259-267
1980 Bacterial turgor pressure can be measured by atomic force microscopy
M. Arnoldi, M. Fritz, E. Bauerlein, M. Radmacher, E. Sackmann, A. Boulbitch
Phys. Rev. E: Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics, 62 (2000) 1/B, 1034-1044
2000 Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils
J. C. Thimm, D. J. Burritt, W. A. Ducker, L. D. Melton
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1951 Atomic force microscopy of the cell nucleus
L. F. Jimenez-Garcia, R. Fragoso-Soriano
J. Struct. Biol., 129 (2000) 2-3, 218-222
2343 Plasmodium falciparum-infected erythrocytes: qualitative and quantitative analyses of parasite-induced knobs by atomic force microscopy
E. Nagao, O. Kaneko, J. A. Dvorak
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1923 Atomic force microscopy imaging of living cells: a preliminary study of the disruptive effect of the cantilever tip on cell morphology
H. X. You, J. M. Lau, S. Zhang, L. Yu
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2111 Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton
H. Haga, S. Sasaki, K. Kawabata, E. Ito, T. Ushiki, T. Sambongi
Ultramicroscopy, 82 (2000) 1-4, 253-258
2275 Mechanical stimulation of individual stereocilia of living cochlear hair cells by atomic force microscopy
M. G. Langer, A. Koitschev, H. Haase, U. Rexhausen, J. K. Horber, J. P. Ruppersberg
Ultramicroscopy, 82 (2000) 1-4, 269-278
2341 Plasma membrane plasticity of Xenopus laevis oocyte imaged with atomic force microscopy
H. Schillers, T. Danker, H. J. Schnittler, F. Lang, H. Oberleithner
Cell. Physiol. Biochem., 10 (2000) 1-2, 99-107
2472 Tapping-mode atomic force microscopy on intact cells: optimal adjustment of tapping conditions by using the deflection signal
V. Vie, M. C. Giocondi, E. Lesniewska, E. Finot, J. P. Goudonnet, C. Le Grimellec
Ultramicroscopy, 82 (2000) 1-4, 279-288
1842 Volume dynamics in migrating epithelial cells measured with atomic force microscopy
S. W. Schneider, P. Pagel, C. Rotsch, T. Danker, H. Oberleithner, M. Radmacher, A. Schwab
Pflugers. Arch., 439 (2000) 3, 297-303
2251 Local mechanical properties measured by atomic force microscopy for cultured bovine endothelial cells exposed to shear stress
M. Sato, K. Nagayama, N. Kataoka, M. Sasaki, K. Hane
J. Biomech., 33 (2000) 1, 127-135
2292 Molecular basis of cell adhesion to polymers characterized AFM
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1861 Adapting atomic force microscopy for cell biology
P. P. Lehenkari, G. T. Charras, A. Nykanen, M. A. Horton
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2558 Volume dynamics in migrating epithelial cells measured with atomic force microscopy
S. W. Schneider, P. Pagel, C. Rotsch, T. Danker, H. Oberleithner, M. Radmacher, A. Schwab
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1913 Atomic force microscopy can be used to mechanically stimulate osteoblasts and evaluate cellular strain distributions
G. T. Charras, P. P. Lehenkari, M. A. Horton
Ultramicroscopy, 86 (2001) 1-2, 85-95
2359 Quantification of red blood cells using atomic force microscopy
M. O'Reilly, L. McDonnell, J. O'Mullane
Ultramicroscopy, 86 (2001) 1-2, 107-112
1952 Atomic force microscopy of the erythrocyte membrane skeleton
A. H. Swihart, J. M. Mikrut, J. B. Ketterson, R. C. Macdonald
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1895 Application of atomic force microscopy to microbial surfaces: from reconstituted cell surface layers to living cells
Y. F. Dufrene
Micron, 32 (2001) 2, 153-165
2351 Probing molecular interactions and mechanical properties of microbial cell surfaces by atomic force microscopy
Y. F. Dufrene, C. J. P. Boonaert, H. C. van der Mei, H. J. Busscher, P. G. Rouxhet
Ultramicroscopy, 86 (2001) 1-2, 113-120
1899 Artificially induced unusual shape of erythrocytes: an atomic force microscopy study
M. Girasole, A. Cricenti, R. Generosi, A. Congiu-Castellano, G. Boumis, G. Amiconi
J. Microsc., 204 (2001) 1, 46-52
2382 Scanning force microscopy observation of tumor cells treated with hematoporphyrin IX derivatives
R. Bischoff, G. Bischoff, S. Hoffmann
Ann. Biomed. Eng., 29 (2001) 12, 1092-1099
2166 High-Q dynamic force microscopy in liquid and its application to living cells
J. Tamayo, A. D. Humphris, R. J. Owen, M. J. Miles
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1966 Atomic Force Microscopy Study of the Adhesion of Saccharomyces cerevisiae
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1993 Blood cell adhesion on sensor materials studied by light, scanning electron, and atomic-force microscopy
G. Hildebrand, S. Kunze, M. Driver
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2252 Local mechanical properties of guinea pig outer hair cells measured by atomic force microscopy
M. Sugawara, Y. Ishida, H. Wada
Hear Res., 174 (2002) 1-2, 222-229
1942 Atomic force microscopy of height fluctuations of fibroblast cells
B. Szabo, D. Selmeczi, Z. Kornyei, E. Madarasz, N. Rozlosnik
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2348 Potassium-selective atomic force microscopy on ion-releasing substrates and living cells
P. Schar-Zammaretti, U. Ziegler, I. Forster, P. Groscurth, U. E. Spichiger-Keller
Anal. Chem., 74 (2002) 16, 4269-4274
2243 Lamellar subcomponents of the cuticular cell membrane complex of mammalian keratin fibres show friction and hardness contrast by AFM
J. R. Smith, J. A. Swift
J. Microsc., 206 (2002) 3, 182-193
2478 The biophysics of sensory cells of the inner ear examined by atomic force microscopy and patch clamp
M. G. Langer, A. Koitschev
Methods Cell Biol., 68 (2002) 141-169
2226 Investigating live and fixed epithelial and fibroblast cells by atomic force microscopy
K. Sinniah, J. Paauw, J. Ubels
Curr. Eye. Res., 24 (2002) 3, 188-195
2169 High-resolution three-dimensional imaging of the lateral plasma membrane of cochlear outer hair cells by atomic force microscopy
C. Le Grimellec, M. C. Giocondi, M. Lenoir, M. Vater, G. Sposito, R. Pujol
J. Comp. Neurol., 451 (2002) 1, 62-69
2132 Experimental and numerical analyses of local mechanical properties measured by atomic force microscopy for sheared endothelial cells
T. Ohashi, Y. Ishii, Y. Ishikawa, T. Matsumoto, M. Sato
Biomed. Mater. Eng., 12 (2002) 3, 319-327
2017 Characterization of the adhesive mucilages secreted by live diatom cells using atomic force microscopy
M. J. Higgins, S. A. Crawford, P. Mulvaney, R. Wetherbee
Protist, 153 (2002) 1, 25-38