Biological AFM: where we come from – where we are – where we may go

Biological atomic force microscopy (AFM) is a fast growing and advancing field. This review's objective is to overview the state of the art and to retrace achievements of biological AFM as presented by past and present research, and wishes to give a (subjective) outlook where AFM may go in the upcoming years. The following areas of interest are discussed: High‐resolution imaging, cell imaging, single molecule force spectroscopy, cell mechanical measurements, combined AFM instrumentation, and AFM instrumentation. Of all these topics, particular representative examples are shown, each of them standing for a variety of achievements by many research groups. Copyright © 2011 John Wiley & Sons, Ltd.

[1]  Mervyn J Miles,et al.  A mechanical microscope: High speed atomic force microscopy , 2005 .

[2]  S. Hell,et al.  STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis , 2006, Nature.

[3]  Isao Shimoyama,et al.  Direct measurement of the binding force between microfabricated particles and a planar surface in aqueous solution by force-sensing piezoresistive cantilevers. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[4]  J. Hoh,et al.  Slow cellular dynamics in MDCK and R5 cells monitored by time-lapse atomic force microscopy. , 1994, Biophysical journal.

[5]  N. Gavara,et al.  Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  D. Klenerman,et al.  Nanoscale live-cell imaging using hopping probe ion conductance microscopy , 2009, Nature Methods.

[7]  M. Rief,et al.  Reversible unfolding of individual titin immunoglobulin domains by AFM. , 1997, Science.

[8]  S. Scheuring,et al.  Automated setpoint adjustment for biological contact mode atomic force microscopy imaging , 2010, Nanotechnology.

[9]  Toshio Ando,et al.  Dynamics of bacteriorhodopsin 2D crystal observed by high-speed atomic force microscopy. , 2009, Journal of structural biology.

[10]  Hermann Schillers,et al.  Plasma sodium stiffens vascular endothelium and reduces nitric oxide release , 2007, Proceedings of the National Academy of Sciences.

[11]  A. Engel,et al.  Native Escherichia coli OmpF porin surfaces probed by atomic force microscopy. , 1995, Science.

[12]  M. Rief,et al.  The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy. , 1998, Biophysical journal.

[13]  Chikashi Nakamura,et al.  Nanoscale operation of a living cell using an atomic force microscope with a nanoneedle. , 2005, Nano letters.

[14]  Jizhong Lou,et al.  Force history dependence of receptor-ligand dissociation. , 2005, Biophysical journal.

[15]  P K Hansma,et al.  Stepwise unfolding of titin under force-clamp atomic force microscopy. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Paul K. Hansma,et al.  Tapping mode atomic force microscopy in liquids , 1994 .

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

[18]  N. Spencer,et al.  Sensitivity of Frictional Forces to pH on a Nanometer Scale: A Lateral Force Microscopy Study , 1995 .

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

[20]  Thomas Walz,et al.  The supramolecular architecture of junctional microdomains in native lens membranes , 2007, EMBO reports.

[21]  Ricardo Garcia,et al.  Force microscopy imaging of individual protein molecules with sub‐pico Newton force sensitivity , 2007, Journal of molecular recognition : JMR.

[22]  C. Stock,et al.  Simultaneous mechanical stiffness and electrical potential measurements of living vascular endothelial cells using combined atomic force and epifluorescence microscopy , 2009, Nanotechnology.

[23]  Takeshi Fukuma,et al.  Development of liquid-environment frequency modulation atomic force microscope with low noise deflection sensor for cantilevers of various dimensions , 2006 .

[24]  J. Rao,et al.  Nanomechanical analysis of cells from cancer patients. , 2007, Nature nanotechnology.

[25]  C. le Grimellec,et al.  Imaging of the surface of living cells by low-force contact-mode atomic force microscopy. , 1998, Biophysical journal.

[26]  Gerber,et al.  Atomic Force Microscope , 2020, Definitions.

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

[28]  Olav Solgaard,et al.  An atomic force microscope tip designed to measure time-varying nanomechanical forces , 2007, Nature Nanotechnology.

[29]  N. Gavara,et al.  Rheology of passive and adhesion-activated neutrophils probed by atomic force microscopy. , 2006, Biophysical journal.

[30]  M Radmacher,et al.  Measuring the elastic properties of biological samples with the AFM. , 1997, IEEE engineering in medicine and biology magazine : the quarterly magazine of the Engineering in Medicine & Biology Society.

[31]  H. Gaub,et al.  Ultrastable combined atomic force and total internal reflection fluorescence microscope [corrected]. , 2009, The Review of scientific instruments.

[32]  C D Woodworth,et al.  Atomic force microscopy detects differences in the surface brush of normal and cancerous cells. , 2009, Nature nanotechnology.

[33]  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.

[34]  Midhat H Abdulreda,et al.  Force spectroscopy of LFA-1 and its ligands, ICAM-1 and ICAM-2. , 2006, Biomacromolecules.

[35]  Christian Hafner,et al.  Nanoscale roughness on metal surfaces can increase tip-enhanced Raman scattering by an order of magnitude. , 2007, Nano letters.

[36]  I. Tinoco,et al.  Equilibrium Information from Nonequilibrium Measurements in an Experimental Test of Jarzynski's Equality , 2002, Science.

[37]  J. Vesenka,et al.  Combining optical and atomic force microscopy for life sciences research. , 1995, BioTechniques.

[38]  Toshio Ando,et al.  (www.interscience.wiley.com) DOI:10.1002/jmr.843 Review , 2022 .

[39]  P K Hansma,et al.  Direct observation of one-dimensional diffusion and transcription by Escherichia coli RNA polymerase. , 1999, Biophysical journal.

[40]  V. Svetlic̆ić,et al.  Biophysical Scenario of Giant Gel Formation in the Northern Adriatic Sea , 2005, Annals of the New York Academy of Sciences.

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

[42]  Dieter Oesterhelt,et al.  Stability of Bacteriorhodopsin α-Helices and Loops Analyzed by Single-Molecule Force Spectroscopy , 2002 .

[43]  C. Jarzynski.  Nonequilibrium Equality for Free Energy Differences , 1996, cond-mat/9610209.

[44]  Daniel J. Muller,et al.  Locating ligand binding and activation of a single antiporter , 2005, EMBO reports.

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

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

[47]  Sergio Marco,et al.  Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Engel,et al.  Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope. , 1999, Biophysical journal.

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

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

[51]  M. Stark,et al.  Stabilized atomic force microscopy imaging in liquids using second harmonic of cantilever motion for setpoint control , 2004 .

[52]  U. Schwarz,et al.  Dynamic force spectroscopy on multiple bonds: Experiments and model , 2007, 0712.3042.

[53]  H. E. de Wardener,et al.  Potassium softens vascular endothelium and increases nitric oxide release , 2009, Proceedings of the National Academy of Sciences.

[54]  Ricardo Henriques,et al.  PALM and STORM: What hides beyond the Rayleigh limit? , 2009, Biotechnology journal.

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

[56]  Yves F Dufrêne,et al.  In vivo imaging of S-layer nanoarrays on Corynebacterium glutamicum. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[57]  S. Lindsay,et al.  A magnetically driven oscillating probe microscope for operation in liquids , 1996 .

[58]  Thomas Walz,et al.  The advent of near-atomic resolution in single-particle electron microscopy. , 2009, Annual review of biochemistry.

[59]  Gil U. Lee,et al.  Direct measurement of the forces between complementary strands of DNA. , 1994, Science.

[60]  R. Henderson,et al.  Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. , 1990, Journal of molecular biology.

[61]  H. Gaub,et al.  Unfolding pathways of individual bacteriorhodopsins. , 2000, Science.

[62]  Daniel J Müller,et al.  Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy. , 2002, Biophysical journal.

[63]  D. Navajas,et al.  Cell dynamic adhesion and elastic properties probed with cylindrical atomic force microscopy cantilever tips , 2007, Journal of molecular recognition : JMR.

[64]  Helmut Grubmüller,et al.  Force spectroscopy of single biomolecules. , 2002, Chemphyschem : a European journal of chemical physics and physical chemistry.

[65]  C. Kiang,et al.  Experimental free energy surface reconstruction from single-molecule force spectroscopy using Jarzynski's equality. , 2007, Physical review letters.

[66]  V. Moy,et al.  Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction. , 2002, Biophysical journal.

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

[68]  M. Hegner,et al.  Specific antigen/antibody interactions measured by force microscopy. , 1996, Biophysical journal.

[69]  P. Arratia,et al.  Absence of filamin A prevents cells from responding to stiffness gradients on gels coated with collagen but not fibronectin. , 2009, Biophysical journal.

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

[71]  A. Engel,et al.  Atomic-force microscopy: Rhodopsin dimers in native disc membranes , 2003, Nature.

[72]  Cheng Zhu,et al.  JCB_200810002 1275..1284 , 2009 .

[73]  F. MacKintosh,et al.  Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. , 2000, Physical review letters.

[74]  Daniel J. Muller,et al.  Free energy of membrane protein unfolding derived from single-molecule force measurements. , 2007, Biophysical journal.

[75]  Ricardo Garcia,et al.  Identification of nanoscale dissipation processes by dynamic atomic force microscopy. , 2006, Physical review letters.

[76]  P. Lehenkari,et al.  Adapting atomic force microscopy for cell biology. , 2000, Ultramicroscopy.

[77]  Farshid Guilak,et al.  A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? , 2007, Biophysical journal.

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

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

[80]  Simon Scheuring,et al.  Chromatic Adaptation of Photosynthetic Membranes , 2005, Science.

[81]  Yves F Dufrêne,et al.  Unfolding individual als5p adhesion proteins on live cells. , 2009, ACS nano.

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

[83]  H Schindler,et al.  Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[85]  Ami Chand,et al.  Probing protein–protein interactions in real time , 2000, Nature Structural Biology.

[86]  Pierre Sens,et al.  Experimental evidence for membrane-mediated protein-protein interaction. , 2010, Biophysical journal.

[87]  W. H. Goldmann,et al.  Differences in elasticity of vinculin-deficient F9 cells measured by magnetometry and atomic force microscopy. , 1998, Experimental cell research.

[88]  T. Ando,et al.  Anisotropic diffusion of point defects in a two-dimensional crystal of streptavidin observed by high-speed atomic force microscopy , 2008, Nanotechnology.

[89]  M. Radmacher,et al.  Imaging viscoelasticity by force modulation with the atomic force microscope. , 1993, Biophysical journal.

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

[91]  P K Hansma,et al.  Imaging the membrane protein bacteriorhodopsin with the atomic force microscope. , 1990, Biophysical journal.

[92]  Ben Fabry,et al.  Microrheology of human lung epithelial cells measured by atomic force microscopy. , 2003, Biophysical journal.

[93]  Z. Shao,et al.  Chaperonins GroEL and GroES: views from atomic force microscopy. , 1996, Biophysical journal.

[94]  Angelika A Noegel,et al.  A mechanical unfolding intermediate in an actin-crosslinking protein , 2004, Nature Structural &Molecular Biology.

[95]  S Lees,et al.  Measuring the microelastic properties of biological material. , 1992, Biophysical journal.

[96]  Ferenc Horkay,et al.  Determination of elastic moduli of thin layers of soft material using the atomic force microscope. , 2002, Biophysical journal.

[97]  S. Scheuring,et al.  Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery , 2009, Photosynthesis Research.

[98]  Ashley R. Carter,et al.  Ultrastable atomic force microscopy: atomic-scale stability and registration in ambient conditions. , 2009, Nano letters.

[99]  H. Gaub,et al.  Adhesion forces between individual ligand-receptor pairs. , 1994, Science.

[100]  M. Dong,et al.  Determination of protein structural flexibility by microsecond force spectroscopy. , 2009, Nature nanotechnology.