AFM and FluidFM Technologies: Recent Applications in Molecular and Cellular Biology

Atomic force microscopy (AFM) is a widely used imaging technique in material sciences. After becoming a standard surface-imaging tool, AFM has been proven to be useful in addressing several biological issues such as the characterization of cell organelles, quantification of DNA-protein interactions, cell adhesion forces, and electromechanical properties of living cells. AFM technique has undergone many successful improvements since its invention, including fluidic force microscopy (FluidFM), which combines conventional AFM with microchanneled cantilevers for local liquid dispensing. This technology permitted to overcome challenges linked to single-cell analyses. Indeed, FluidFM allows isolation and injection of single cells, force-controlled patch clamping of beating cardiac cells, serial weighting of micro-objects, and single-cell extraction for molecular analyses. This work aims to review the recent studies of AFM implementation in molecular and cellular biology.

[1]  J. Vorholt,et al.  Isolation of Optically Targeted Single Bacteria by Application of Fluidic Force Microscopy to Aerobic Anoxygenic Phototrophs from the Phyllosphere , 2013, Applied and Environmental Microbiology.

[2]  Adarsh Krishnamurthy,et al.  Novel role for vinculin in ventricular myocyte mechanics and dysfunction. , 2013, Biophysical journal.

[3]  David J. Hodson,et al.  New Understanding of β-Cell Heterogeneity and In Situ Islet Function , 2018, Diabetes.

[4]  B. Codan,et al.  The Cardiomyopathy Lamin A/C D192G Mutation Disrupts Whole-Cell Biomechanics in Cardiomyocytes as Measured by Atomic Force Microscopy Loading-Unloading Curve Analysis , 2015, Scientific Reports.

[5]  T. Berney,et al.  Insulin secretion from human beta cells is heterogeneous and dependent on cell-to-cell contacts , 2008, Diabetologia.

[6]  H. McBride,et al.  In vivo and in vitro examination of the functional significances of novel lamin gene mutations in heart failure patients , 2005, Journal of Medical Genetics.

[7]  J. Vorholt,et al.  Cooperative vaccinia infection demonstrated at the single-cell level using FluidFM. , 2012, Nano letters.

[8]  C. Gerber,et al.  Surface Studies by Scanning Tunneling Microscopy , 1982 .

[9]  C. C. Toma,et al.  Morphomechanical and structural changes induced by ROCK inhibitor in breast cancer cells , 2017, Experimental cell research.

[10]  E. Zaklyazminskaya,et al.  Cardiac channelopathies: genetic and molecular mechanisms. , 2013, Gene.

[11]  J. Senard,et al.  Biophysical properties of cardiomyocyte surface explored by multiparametric AFM. , 2017, Journal of structural biology.

[12]  M. Vassalli,et al.  Serial weighting of micro-objects with resonant microchanneled cantilevers , 2016, Nanotechnology.

[13]  Tomaso Zambelli,et al.  Isolation of single mammalian cells from adherent cultures by fluidic force microscopy. , 2014, Lab on a chip.

[14]  B. Van Houten,et al.  Studying protein-DNA interactions using atomic force microscopy. , 2018, Seminars in cell & developmental biology.

[15]  Tomaso Zambelli,et al.  Tunable Single-Cell Extraction for Molecular Analyses , 2016, Cell.

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

[17]  T. Konry,et al.  Quantification of intercellular adhesion forces measured by fluid force microscopy. , 2017, Talanta.

[18]  M. Amarouch,et al.  Cellular hyper-excitability caused by mutations that alter the activation process of voltage-gated sodium channels , 2015, Front. Physiol..

[19]  Bobo Huang,et al.  Study of the union method of microelectrode array and AFM for the recording of electromechanical activities in living cardiomyocytes , 2017, European Biophysics Journal.

[20]  G. Dietler,et al.  DNA-protein interactions explored by atomic force microscopy. , 2018, Seminars in cell & developmental biology.

[21]  J. Vorholt,et al.  Single-Cell Mass Spectrometry of Metabolites Extracted from Live Cells by Fluidic Force Microscopy. , 2017, Analytical chemistry.

[22]  N. Amer,et al.  Novel optical approach to atomic force microscopy , 1988 .

[23]  L. Hellman,et al.  Electrophoretic mobility shift assay (EMSA) for detecting protein–nucleic acid interactions , 2007, Nature Protocols.

[24]  Braet,et al.  Imaging surface and submembranous structures with the atomic force microscope: a study on living cancer cells, fibroblasts and macrophages , 1998, Journal of microscopy.

[25]  J. Rougier,et al.  TRPM4 channels in the cardiovascular system: physiology, pathophysiology, and pharmacology. , 2012, Biochemical pharmacology.

[26]  Yan Shi,et al.  The structure and function of cell membranes studied by atomic force microscopy. , 2018, Seminars in cell & developmental biology.

[27]  Tomaso Zambelli,et al.  Force-controlled fluidic injection into single cell nuclei. , 2013, Small.

[28]  A. Becker,et al.  Specific binding of the regulatory protein ExpG to promoter regions of the galactoglucan biosynthesis gene cluster of Sinorhizobium meliloti--a combined molecular biology and force spectroscopy investigation. , 2003, Journal of structural biology.

[29]  A Piednoir,et al.  Multi-scale mechanical characterization of prostate cancer cell lines: Relevant biological markers to evaluate the cell metastatic potential. , 2017, Biochimica et biophysica acta. General subjects.

[30]  Tomaso Zambelli,et al.  Force-controlled patch clamp of beating cardiac cells. , 2015, Nano letters.

[31]  V. Orlando,et al.  Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. , 2000, Trends in biochemical sciences.

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

[33]  M. Lidstrom,et al.  The role of physiological heterogeneity in microbial population behavior. , 2010, Nature chemical biology.

[34]  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.

[35]  J. Kashef,et al.  Cadherin-11 promotes neural crest cell spreading by reducing intracellular tension-Mapping adhesion and mechanics in neural crest explants by atomic force microscopy. , 2018, Seminars in cell & developmental biology.

[36]  H. Carter,et al.  Structure-Based Analysis Reveals Cancer Missense Mutations Target Protein Interaction Interfaces , 2016, PloS one.

[37]  Y. Lyubchenko,et al.  Remodeling of RecG Helicase at the DNA Replication Fork by SSB Protein , 2015, Scientific Reports.

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

[39]  J. Sweedler,et al.  Single Cell Peptide Heterogeneity of Rat Islets of Langerhans. , 2016, ACS chemical biology.

[40]  Yanwei Wang,et al.  Investigating the Influence of Magnesium Ions on p53–DNA Binding Using Atomic Force Microscopy , 2017, International journal of molecular sciences.

[41]  L. A. Baker,et al.  Atomic force microscopy-based bioanalysis for the study of disease , 2014 .

[42]  R. Duval,et al.  Cell biology of microbes and pharmacology of antimicrobial drugs explored by Atomic Force Microscopy. , 2018, Seminars in cell & developmental biology.

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

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