Probing nanomechanical properties from biomolecules to living cells

Atomic force microscopy is being increasingly used to explore the physical properties of biological structures. This technique involves the application of a force to the sample and a monitoring of the ensuing deformation process. The available experimental setups can be broadly divided into two categories, one of which involves a stretching and the other an indentation of the organic materials. In this review, we will focus on the indentation technique and will illustrate its application to biological materials with examples that range from single molecules to living cells.

[1]  Giovanni Dietler,et al.  Gradient of rigidity in the lamellipodia of migrating cells revealed by atomic force microscopy. , 2005, Biophysical journal.

[2]  B. Logan,et al.  Contributions of Bacterial Surface Polymers, Electrostatics, and Cell Elasticity to the Shape of AFM Force Curves , 2002 .

[3]  Bernard Nysten,et al.  Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy , 2003 .

[4]  C Rotsch,et al.  Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. , 2000, Biophysical journal.

[5]  T. Schäffer,et al.  Influence of hydrocortisone on the mechanical properties of the cerebral endothelium in vitro. , 2005, Biophysical journal.

[6]  W S Klug,et al.  Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  O. Marti,et al.  Micromechanical properties of tobacco mosaic viruses , 2007, Journal of microscopy.

[8]  Atsushi Ikai.  Local rigidity of a protein molecule. , 2005, Biophysical chemistry.

[9]  J. Hoh,et al.  Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy , 1996 .

[10]  C. S. Chen,et al.  Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Gil U. Lee,et al.  High-resolution analysis of neuronal growth cone morphology by comparative atomic force and optical microscopy. , 2006, Journal of neurobiology.

[12]  Hiroshi Sekiguchi,et al.  Pulling and Pushing Protein Molecules by AFM , 2007 .

[13]  Diane J. Burgess,et al.  Rate- and depth-dependent nanomechanical behavior of individual living Chinese hamster ovary cells probed by atomic force microscopy , 2006 .

[14]  N. Spencer,et al.  Interaction forces and morphology of a protein-resistant poly(ethylene glycol) layer. , 2005, Biophysical journal.

[15]  C. Schmidt,et al.  Resolving the molecular structure of microtubules under physiological conditions with scanning force microscopy , 2004, European Biophysics Journal.

[16]  P. Mulvaney,et al.  THE STRUCTURE AND NANOMECHANICAL PROPERTIES OF THE ADHESIVE MUCILAGE THAT MEDIATES DIATOM‐SUBSTRATUM ADHESION AND MOTILITY 1 , 2003 .

[17]  Z. Stachura,et al.  Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy , 1999, European Biophysics Journal.

[18]  Yuekan Jiao,et al.  Accurate height and volume measurements on soft samples with the atomic force microscope. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[19]  Differential action of steroid hormones on human endothelium , 2006, Journal of Cell Science.

[20]  Vinod Subramaniam,et al.  Micromechanical bending of single collagen fibrils using atomic force microscopy. , 2007, Journal of biomedical materials research. Part A.

[21]  G. Dietler,et al.  Force-distance curves by atomic force microscopy , 1999 .

[22]  G. Charras,et al.  Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. , 2002, Biophysical journal.

[23]  Giovanni Dietler,et al.  Elastic membrane heterogeneity of living cells revealed by stiff nanoscale membrane domains. , 2008, Biophysical journal.

[24]  C. Lim,et al.  Biomechanics approaches to studying human diseases. , 2007, Trends in biotechnology.

[25]  Kevin D. Costa,et al.  Osteoblast Elastic Modulus Measured by Atomic Force Microscopy Is Substrate Dependent , 2005, Annals of Biomedical Engineering.

[26]  David Barlam,et al.  A stiffness switch in human immunodeficiency virus. , 2007, Biophysical journal.

[27]  H. Wada,et al.  Mechanical properties of sensory and supporting cells in the organ of Corti of the guinea pig cochlea – study by atomic force microscopy , 2004, Hearing Research.

[28]  D L Caspar,et al.  Refined atomic model of the four-layer aggregate of the tobacco mosaic virus coat protein at 2.4-A resolution. , 1998, Biophysical journal.

[29]  K. Bremmell,et al.  Deformation and nano-rheology of red blood cells: an AFM investigation. , 2006, Colloids and Surfaces B: Biointerfaces.

[30]  V. Parpura,et al.  Membrane deformation of living glial cells using atomic force microscopy , 1996, Journal of microscopy.

[31]  T. Gomi,et al.  Imaging of the cortical cytoskeleton of guinea pig outer hair cells using atomic force microscopy 1 1 This study was presented at the 26th Midwinter Research Meeting of the Association for Research in Otolaryngology in February 2003. , 2004, Hearing Research.

[32]  Rehana Afrin,et al.  Pretransition and progressive softening of bovine carbonic anhydrase II as probed by single molecule atomic force microscopy , 2005, Protein science : a publication of the Protein Society.

[33]  Relationship between the local stiffness of the outer hair cell along the cell axis and its ultrastructure observed by atomic force microscopy , 2003, Hearing Research.

[34]  Kevin D. Costa,et al.  Single-Cell Elastography: Probing for Disease with the Atomic Force Microscope , 2004, Disease markers.

[35]  J. M. Fernández,et al.  Atomic force microscopy study of the secretory granule lumen. , 1996, Biophysical journal.

[36]  Félix Pariente,et al.  Nanomechanical properties of globular proteins: lactate oxidase. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[37]  Wojciech Strojny,et al.  Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy. , 2006, Journal of biochemical and biophysical methods.

[38]  Hiroshi Wada,et al.  Local mechanical properties of mouse outer hair cells: atomic force microscopic study. , 2006, Auris, nasus, larynx.

[39]  H. Haga,et al.  Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton. , 2000, Ultramicroscopy.

[40]  Kazuhiro Abe,et al.  Fine Surface Images That Reflect Cytoskeletal Structures in Cultured Glial Cells by Atomic Force Microscopy , 1998 .

[41]  Paul K. Hansma,et al.  Imaging adhesion forces and elasticity of lysozyme adsorbed on mica with the atomic force microscope , 1994 .

[42]  A. Ikai,et al.  Mechanical perturbation-induced fluorescence change of green fluorescent protein , 2005 .

[43]  V. Moy,et al.  Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking. , 2006, Scanning.

[44]  John E. Sader,et al.  PROBING THE SURFACE OF LIVING DIATOMS WITH ATOMIC FORCE MICROSCOPY: THE NANOSTRUCTURE AND NANOMECHANICAL PROPERTIES OF THE MUCILAGE LAYER 1 , 2003 .

[45]  Giovanni Dietler,et al.  Mechanical properties of microtubules explored using the finite elements method. , 2004, Chemphyschem : a European journal of chemical physics and physical chemistry.

[46]  H. Oberleithner.  Aldosterone makes human endothelium stiff and vulnerable. , 2005, Kidney international.

[47]  H. Hansma,et al.  Changes in the elastic properties of cholinergic synaptic vesicles as measured by atomic force microscopy. , 1997, Biophysical journal.

[48]  Peter Young,et al.  AFM combines functional and morphological analysis of peripheral myelinated and demyelinated nerve fibers , 2007, NeuroImage.

[49]  Christoph F Schmidt,et al.  Elastic response, buckling, and instability of microtubules under radial indentation. , 2006, Biophysical journal.

[50]  S Bloom,et al.  Intermediate filament-mediated stretch-induced changes in chromatin: a hypothesis for growth initiation in cardiac myocytes. , 1996, Journal of molecular and cellular cardiology.

[51]  U G Hofmann,et al.  Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope. , 1997, Journal of structural biology.

[52]  P. Lehenkari,et al.  Atomic force microscopy can be used to mechanically stimulate osteoblasts and evaluate cellular strain distributions. , 2001, Ultramicroscopy.

[53]  W. Xu,et al.  Modeling and measuring the elastic properties of an archaeal surface, the sheath of Methanospirillum hungatei, and the implication of methane production , 1996, Journal of bacteriology.

[54]  Zbigniew Stachura,et al.  Local elastic properties of cells studied by SFM , 1999 .

[55]  U. Aebi,et al.  Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. , 2006, Journal of molecular biology.

[56]  Y. Engelborghs,et al.  Immobilizing and imaging microtubules by atomic force microscopy. , 1995, Ultramicroscopy.

[57]  William S Klug,et al.  Nonlinear finite-element analysis of nanoindentation of viral capsids. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  P K Hansma,et al.  Measuring the viscoelastic properties of human platelets with the atomic force microscope. , 1996, Biophysical journal.

[59]  W F Heinz,et al.  Relative microelastic mapping of living cells by atomic force microscopy. , 1998, Biophysical journal.

[60]  P K Hansma,et al.  Micromechanical and structural properties of a pennate diatom investigated by atomic force microscopy , 2001, Journal of microscopy.

[61]  Nicolas H Voelcker,et al.  AFM nanoindentations of diatom biosilica surfaces. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[62]  W. Roos,et al.  Viral capsids: Mechanical characteristics, genome packaging and delivery mechanisms , 2007, Cellular and Molecular Life Sciences.

[63]  R. Scheller,et al.  Synaptic vesicle biogenesis, docking, and fusion: a molecular description. , 1996, Physiological reviews.

[64]  Manfred H. Jericho,et al.  Atomic force microscopy and theoretical considerations of surface properties and turgor pressures of bacteria , 2002 .

[65]  C Rotsch,et al.  EGF-stimulated lamellipod extension in adenocarcinoma cells. , 2001, Ultramicroscopy.

[66]  M. Bradbury,et al.  The blood-brain barrier in vitro , 1985, Neurochemistry International.

[67]  G. Drewes,et al.  MAPs, MARKs and microtubule dynamics. , 1998, Trends in biochemical sciences.

[68]  Zachary J. Donhauser,et al.  Enhanced mechanical stability of microtubules polymerized with a slowly hydrolyzable nucleotide analogue. , 2007, The journal of physical chemistry. B.

[69]  Ferry Kienberger,et al.  Vacuolar structures can be identified by AFM elasticity mapping. , 2007, Ultramicroscopy.

[70]  H. Butt,et al.  Force measurements with the atomic force microscope: Technique, interpretation and applications , 2005 .

[71]  E. Dague,et al.  Surface Structure and Nanomechanical Properties of Shewanella putrefaciens Bacteria at Two pH values (4 and 10) Determined by Atomic Force Microscopy , 2005, Journal of bacteriology.

[72]  M. Lekka,et al.  Erythrocyte stiffness in diabetes mellitus studied with atomic force microscope. , 2006, Clinical hemorheology and microcirculation.

[73]  M. Kirschner,et al.  Dynamic instability of microtubule growth , 1984, Nature.

[74]  F. MacKintosh,et al.  Deformation and collapse of microtubules on the nanometer scale. , 2003, Physical review letters.

[75]  J. Janda,et al.  Biochemical and Pathogenic Properties ofShewanella alga and Shewanella putrefaciens , 1998, Journal of Clinical Microbiology.

[76]  Giovanni Dietler,et al.  Techniques for measuring microtubule stiffness , 2007 .

[77]  C. Schmidt,et al.  Tau protein binding forms a 1 nm thick layer along protofilaments without affecting the radial elasticity of microtubules. , 2007, Journal of structural biology.

[78]  Daniel J Müller,et al.  Analyzing focal adhesion structure by atomic force microscopy , 2005, Journal of Cell Science.

[79]  L. Forró,et al.  Superficial and deep changes of cellular mechanical properties following cytoskeleton disassembly. , 2005, Cell motility and the cytoskeleton.

[80]  C. Schönenberger,et al.  Nanomechanics of microtubules. , 2002, Physical review letters.

[81]  T. Camesano,et al.  Polysaccharide properties probed with atomic force microscopy , 2003, Journal of microscopy.

[82]  Yves F Dufrêne,et al.  Atomic force microscopy of microbial cells: application to nanomechanical properties, surface forces and molecular recognition forces. , 2007, Colloids and surfaces. B, Biointerfaces.

[83]  Bengt Jönsson,et al.  Internal DNA pressure modifies stability of WT phage , 2007, Proceedings of the National Academy of Sciences.

[84]  A. Ikai,et al.  Observation of the destruction of biomolecules under compression force , 2005 .

[85]  Xuemei Liang,et al.  Probing small unilamellar EggPC vesicles on mica surface by atomic force microscopy. , 2004, Colloids and surfaces. B, Biointerfaces.

[86]  José Luis Alonso,et al.  Feeling the forces: atomic force microscopy in cell biology. , 2003, Life sciences.

[87]  H. Wada,et al.  Local mechanical properties of guinea pig outer hair cells measured by atomic force microscopy 1 1 This study was presented at the 25th Midwinter Research Meeting of the Association for Research in Otolaryngology in January 2002. , 2002, Hearing Research.

[88]  M. Welte,et al.  Bidirectional Transport along Microtubules , 2004, Current Biology.

[89]  K. Yoshikawa,et al.  Relationship between Apical Membrane Elasticity and Stress Fiber Organization in Fibroblasts Analyzed by Fluorescence and Atomic Force Microscopy , 2006, Biomechanics and modeling in mechanobiology.

[90]  Experimental and numerical analyses of local mechanical properties measured by atomic force microscopy for sheared endothelial cells. , 2002, Bio-medical materials and engineering.

[91]  J. Trojanowski,et al.  Neurodegenerative tauopathies. , 2001, Annual review of neuroscience.

[92]  C. Knobler,et al.  Failure of viral shells. , 2006, Physical review letters.

[93]  O. Teschke,et al.  Dynamics of the Antimicrobial Peptide PGLa Action on Escherichia coli Monitored by Atomic Force Microscopy , 2005 .

[94]  David Barlam,et al.  Mechanical properties of murine leukemia virus particles: effect of maturation. , 2006, Biophysical journal.

[95]  C. Rotsch,et al.  AFM IMAGING AND ELASTICITY MEASUREMENTS ON LIVING RAT LIVER MACROPHAGES , 1997, Cell biology international.

[96]  O. Teschke,et al.  Effects of the antimicrobial peptide PGLa on live Escherichia coli. , 2003, Biochimica et biophysica acta.

[97]  A. Ikai.  The world of nano-biomechanics , 2007 .

[98]  Xuemei Liang,et al.  Mechanical properties and stability measurement of cholesterol-containing liposome on mica by atomic force microscopy. , 2004, Journal of colloid and interface science.

[99]  K. Costa,et al.  Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy. , 1999, Journal of biomechanical engineering.