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Atomic Force Microscopy As A Multifunctional Molecular Toolbox In Nanobiotechnology.

D. Müller, Y. Dufrêne
Published 2008 · Materials Science, Medicine, Engineering

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With its ability to observe, manipulate and explore the functional components of the biological cell at subnanometre resolution, atomic force microscopy (AFM) has produced a wealth of new opportunities in nanobiotechnology. Evolving from an imaging technique to a multifunctional 'lab-on-a-tip', AFM-based force spectroscopy is increasingly used to study the mechanisms of molecular recognition and protein folding, and to probe the local elasticity, chemical groups and dynamics of receptor-ligand interactions in live cells. AFM cantilever arrays allow the detection of bioanalytes with picomolar sensitivity, opening new avenues for medical diagnostics and environmental monitoring. Here we review the fascinating opportunities offered by the rapid advances in AFM.
This paper references
10.1038/NMAT776
The myosin coiled-coil is a truly elastic protein structure
I. Schwaiger (2002)
10.1038/NMAT858
Molecular nanosprings in spider capture-silk threads
N. Becker (2003)
10.1021/NL071476K
Chemical force microscopy of single live cells.
E. Dague (2007)
10.1038/nsb965
The mechanical stability of ubiquitin is linkage dependent
M. Carrión-Vázquez (2003)
The nanostructure and nanomechanical properties of the mucilage layer
M. J. Higgins (2003)
10.2174/1389201023378418
Pore-forming proteins and their application in biotechnology.
R. Panchal (2002)
10.1038/sj.emboj.7601326
Fast‐scanning atomic force microscopy reveals the ATP/ADP‐dependent conformational changes of GroEL
M. Yokokawa (2006)
10.1038/sj.embor.7400517
The c15 ring of the Spirulina platensis F‐ATP synthase: F1/F0 symmetry mismatch is not obligatory
D. Pogoryelov (2005)
10.1201/9781420086836.ch15
Past, present--and future?
D. Holdstock (2005)
Atomic probe microscopy on OmpF porin
Philippsen (2002)
10.1016/S0006-3495(03)74940-6
Force Measurements of the α5β1 Integrin–Fibronectin Interaction
F. Li (2003)
10.1091/MBC.E06-09-0777
Revealing Early Steps of α2β1 Integrin-mediated Adhesion to Collagen Type I by Using Single-Cell Force Spectroscopy
A. Taubenberger (2007)
10.1088/0957-4484/14/1/319
Label-free protein assay based on a nanomechanical cantilever array
Y. Arntz (2003)
10.1038/sj.embor.7400455
Locating ligand binding and activation of a single antiporter
A. Kedrov (2005)
10.1038/nnano.2006.70
How the doors to the nanoworld were opened
C. Gerber (2006)
10.1126/SCIENCE.282.5390.902
Force and velocity measured for single molecules of RNA polymerase.
M. Wang (1998)
10.1038/nmeth769
Nanoscale mapping and functional analysis of individual adhesins on living bacteria
V. Duprès (2005)
10.1038/nbt0901-856
Bioassay of prostate-specific antigen (PSA) using microcantilevers
G. Wu (2001)
10.1038/77936
Probing protein–protein interactions in real time
M. Viani (2000)
10.1016/S0006-3495(00)76614-8
Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study.
C. Rotsch (2000)
Revealing early steps of alpha2beta1 integrin-mediated adhesion to collagen type I by using single-cell force spectroscopy.
A. Taubenberger (2007)
10.1016/j.cub.2007.08.063
Straight GDP-Tubulin Protofilaments Form in the Presence of Taxol
C. Elie-Caille (2007)
10.1038/nature02261
Protein folding and misfolding
C. Dobson (2003)
10.1038/nature05741
Weighing of biomolecules, single cells and single nanoparticles in fluid
T. Burg (2007)
10.1038/nnano.2007.388
Nanomechanical analysis of cells from cancer patients.
S. E. Cross (2007)
10.1038/35093038
Stochastic sensors inspired by biology
H. Bayley (2001)
10.1021/LA00014A003
Sensing Discrete Streptavidin-Biotin Interactions with Atomic Force Microscopy
G. Lee (1994)
10.1016/J.JMB.2007.11.032
Examining the dynamic energy landscape of an antiporter upon inhibitor binding.
A. Kedrov (2008)
10.1038/nsb968
Pulling geometry defines the mechanical resistance of a β-sheet protein
D. Brockwell (2003)
10.1088/2058-7058/17/11/34
Molecular devices and machines
V. Balzani (2003)
10.1073/PNAS.95.21.12283
Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy.
J. Fritz (1998)
10.1038/35078583
Direct, high-resolution measurement of furrow stiffening during division of adherent cells
R. Matzke (2001)
10.1529/BIOPHYSJ.107.116491
High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia.
E. Dague (2008)
10.1021/LA702765C
Direct measurement of hydrophobic forces on cell surfaces using AFM.
D. Alsteens (2007)
10.1021/NL0347435
Molecular Shuttles Operating Undercover: A New Photolithographic Approach for the Fabrication of Structured Surfaces Supporting Directed Motility
H. Hess (2003)
10.1038/nnano.2006.134
Rapid and label-free nanomechanical detection of biomarker transcripts in human RNA
J. Zhang (2006)
10.1017/S1431927607070067
An antibody-sensitized microfabricated cantilever for the growth detection of Aspergillus niger spores.
N. Nugaeva (2007)
10.1111/j.1462-2920.2007.01551.x
Nanostructure and nanomechanics of live Phaeodactylum tricornutum morphotypes.
G. Francius (2008)
10.1016/J.SBI.2006.06.001
Single-molecule studies of membrane proteins.
D. Müller (2006)
10.1016/J.JMB.2007.04.073
The supramolecular assemblies of voltage-dependent anion channels in the native membrane.
B. Hoogenboom (2007)
10.1021/NL0700853
Single-molecule force spectroscopy and imaging of the vancomycin/D-Ala-D-Ala interaction.
Yann Gilbert (2007)
10.1103/physrevlett.56.930
Atomic force microscope.
Binnig (1986)
10.1021/BI9624402
Escherichia coli RNA polymerase activity observed using atomic force microscopy.
S. Kasas (1997)
10.1016/J.ACTBIO.2007.04.002
Biomechanics and biophysics of cancer cells.
S. Suresh (2007)
Nanobiotechnology: Concepts, Applications and Perspectives (Wiley-VCH
C. M. Niemeyer (2004)
10.1016/S0006-3495(96)79602-9
Measuring the viscoelastic properties of human platelets with the atomic force microscope.
M. Radmacher (1996)
10.1088/1742-6596/61/1/090
Analyzing Gene Expression Using Combined Nanomechanical Cantilever Sensors
F. Huber (2007)
10.1126/SCIENCE.1092497
Force-Clamp Spectroscopy Monitors the Folding Trajectory of a Single Protein
J. Fernández (2004)
10.1007/s00424-007-0386-0
Organization of the mycobacterial cell wall: a nanoscale view
D. Alsteens (2007)
Conf
Huber (2007)
Force measurements of the alpha5beta1 integrin-fibronectin interaction.
F. Li (2003)
10.1073/pnas.0602995103
Anisotropic deformation response of single protein molecules
H. Dietz (2006)
10.1038/16403
A single myosin head moves along an actin filament with regular steps of 5.3 nanometres
K. Kitamura (1999)
10.1126/science.1151424
Single-Molecule Cut-and-Paste Surface Assembly
S. K. Kufer (2008)
10.1038/12898
Antibody recognition imaging by force microscopy
A. Raab (1999)
10.1038/nnano.2007.39
Applications of dip-pen nanolithography.
Khalid S Salaita (2007)
10.1146/ANNUREV.BIOPHYS.36.040306.132640
Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy.
A. Kedrov (2007)
10.1126/SCIENCE.1110879
Chromatic Adaptation of Photosynthetic Membranes
S. Scheuring (2005)
10.1074/jbc.M609317200
Aminosulfonate Modulated pH-induced Conformational Changes in Connexin26 Hemichannels*
Jinshu Yu (2007)
10.1016/S0006-3495(97)78685-5
Atomic force microscope imaging contrast based on molecular recognition.
M. Ludwig (1997)
10.1073/pnas.152330199
Multiple label-free biodetection and quantitative DNA-binding assays on a nanomechanical cantilever array
R. McKendry (2002)
10.1126/SCIENCE.7973628
Direct measurement of the forces between complementary strands of DNA.
G. U. Lee (1994)
10.1088/0957-4484/16/8/001
Assessment of insulated conductive cantilevers for biology and electrochemistry
P. L. Frederix (2005)
10.1371/journal.pbio.0050268
Force-Induced Unfolding of Fibronectin in the Extracellular Matrix of Living Cells
M. Smith (2007)
10.1038/nmeth922
Nanoscale resolution in GFP-based microscopy
K. Willig (2006)
10.1088/0957-4484/4/2/006
Deformation and height anomaly of soft surfaces studied with an AFM
A. L. Weisenhorn (1993)
10.1124/pr.107.07111
Vertebrate Membrane Proteins: Structure, Function, and Insights from Biophysical Approaches
D. Müller (2008)
10.1039/B514700J
Recent progress on nanovehicles.
Yasuhiro Shirai (2006)
10.1126/SCIENCE.2928794
Imaging crystals, polymers, and processes in water with the atomic force microscope.
B. Drake (1989)
10.1088/0957-4484/13/5/202
Nanomechanics from atomic resolution to molecular recognition based on atomic force microscopy technology
H. Lang (2002)
Tensile forces govern germ layer organization during gastrulation
M Krieg (2008)
10.1038/nature04437
Nanospring behaviour of ankyrin repeats
G. Lee (2006)
10.1016/J.BIOS.2005.07.018
Label free analysis of transcription factors using microcantilever arrays.
F. Huber (2006)
10.1002/SIA.2374
Chemical force microscopy of chemical and biological interactions
A. Noy (2006)
10.1038/nmeth871
Detection and localization of single molecular recognition events using atomic force microscopy
P. Hinterdorfer (2006)
10.1038/35014000
Discrete interactions in cell adhesion measured by single-molecule force spectroscopy
M. Benoit (2000)
10.1038/nrmicro905
Using nanotechniques to explore microbial surfaces
Y. Dufrêne (2004)
10.1016/J.CBPA.2003.08.010
Atomic force bio-analytics.
P. L. Frederix (2003)
10.1063/1.1590737
Ultrahigh-speed scanning near-field optical microscopy capable of over 100 frames per second
A. Humphris (2003)
10.2142/BIOPHYS.41.S92_3
A high-speed atomic force microscope for studying biological macromolecules.
T. Ando (2001)
10.1002/3527602453
Nanobiotechnology :concepts, applications and perspectives
C. Niemeyer (2005)
10.1038/421127a
Atomic-force microscopy: Rhodopsin dimers in native disc membranes
D. Fotiadis (2003)
10.1021/LA034136X
Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy
A. Touhami (2003)
Rhodopsin dimers in native disc membranes: Neat rows of paired photon receptors are caught on camera in their natural state
D. Fotiadis (2003)
Pulling geometry defines the mechanical resistance of a beta-sheet protein.
D. Brockwell (2003)
Nanobiotechnology Report of the National Nanotechnology Initiative Workshop, October 9-11, 2003, Arlington, Virginia
V. Vogel (2005)
10.1016/S0006-3495(02)75517-3
Imaging the electrostatic potential of transmembrane channels: atomic probe microscopy of OmpF porin.
A. Philippsen (2002)
10.1073/PNAS.93.8.3477
Detection and localization of individual antibody-antigen recognition events by atomic force microscopy.
P. Hinterdorfer (1996)
10.1126/SCIENCE.276.5315.1109
Reversible unfolding of individual titin immunoglobulin domains by AFM.
M. Rief (1997)
10.1038/NMAT1825
Polyprotein of GB1 is an ideal artificial elastomeric protein.
Yi Cao (2007)
10.1073/PNAS.96.3.921
Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy.
C. Rotsch (1999)
10.1093/emboj/cdf365
Conformational changes in surface structures of isolated connexin 26 gap junctions
D. Müller (2002)
Technical and Cultural Affairs (Interuniversity Poles of Attraction Programme
a nanoscale view
Alsteens (2008)
10.1146/ANNUREV.BIOPHYS.30.1.105
Probing the relation between force--lifetime--and chemistry in single molecular bonds.
E. Evans (2001)
10.1046/j.1529-8817.2003.02163.x
PROBING THE SURFACE OF LIVING DIATOMS WITH ATOMIC FORCE MICROSCOPY: THE NANOSTRUCTURE AND NANOMECHANICAL PROPERTIES OF THE MUCILAGE LAYER 1
M. Higgins (2003)
An Atomic Force Microscopy Study
Y. Lyubchenko (2004)
10.1016/S0006-3495(98)77948-2
Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2.
M. Grandbois (1998)
10.1038/ncb1705
Tensile forces govern germ-layer organization in zebrafish
M. Krieg (2008)
10.1016/J.BIOS.2005.02.004
Micromechanical cantilever array sensors for selective fungal immobilization and fast growth detection.
N. Nugaeva (2005)
10.1021/BI047907K
Oligomerization of G protein-coupled receptors: past, present, and future.
P. S. Park (2004)
10.1016/S0006-3495(01)75881-X
Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation.
R. Best (2001)
10.1002/cphc.200700662
From valleys to ridges: exploring the dynamic energy landscape of single membrane proteins.
H. Janovjak (2008)
10.1038/nnano.2007.63
Native protein nanolithography that can write, read and erase.
A. Tinazli (2007)
10.1529/BIOPHYSJ.107.109751
Nano-scale dynamic recognition imaging on vascular endothelial cells.
L. Chtcheglova (2007)
10.1016/J.JMB.2006.07.049
Differentiating ligand and inhibitor interactions of a single antiporter.
A. Kedrov (2006)
10.1016/0531-5565(92)90018-U
Acknowledgements
(1992)
10.1038/35013148
Structural biology: Proton-powered turbine of a plant motor
H. Seelert (2000)
10.1073/PNAS.98.2.468
Stepwise unfolding of titin under force-clamp atomic force microscopy.
A. Oberhauser (2001)
10.1126/SCIENCE.288.5464.316
Translating biomolecular recognition into nanomechanics.
J. Fritz (2000)
10.1073/pnas.0702668104
Chemomechanical mapping of ligand–receptor binding kinetics on cells
S. Lee (2007)
10.1016/j.jmb.2008.01.085
BCR/ABL expression of myeloid progenitors increases beta1-integrin mediated adhesion to stromal cells.
F. Fierro (2008)
10.1126/science.265.5181.2071
Functional Group Imaging by Chemical Force Microscopy
C. Frisbie (1994)
10.1038/78929
Observing single biomolecules at work with the atomic force microscope
A. Engel (2000)
10.1126/science.7886447
Navigating the folding routes
P. Wolynes (1995)
10.1126/SCIENCE.290.5496.1555
Powering an inorganic nanodevice with a biomolecular motor.
R. Soong (2000)
10.1126/SCIENCE.7939660
Intermolecular forces and energies between ligands and receptors.
V. Moy (1994)



This paper is referenced by
Multi-domain Protein Unfolding Pathway Studies by Single Molecule Techniques
Qing Li (2017)
10.1021/nn5010588
Improved single molecule force spectroscopy using micromachined cantilevers.
M. S. Bull (2014)
10.1038/ncomms7843
Cytosolic targeting factor AKR2A captures chloroplast outer membrane-localized client proteins at the ribosome during translation.
D. H. Kim (2015)
10.1038/nchembio.220
The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo.
V. Duprès (2009)
10.1039/c1cc10778j
A single-molecule study of the inhibition effect of Naringenin on transforming growth factor-β ligand-receptor binding.
Y. Yang (2011)
10.1007/978-1-62703-176-9_24
High-resolution imaging of 2D outer membrane protein F crystals by atomic force microscopy.
D. Fotiadis (2013)
Probing dynamic fibril-formation by an integrated microscopic approach
Y. Cao (2012)
10.1146/annurev-anchem-061417-010055
Single-Molecule Force Spectroscopy of Transmembrane β-Barrel Proteins.
Johannes Thoma (2018)
10.1002/sca.20173
Application of AFM in microbiology: a review.
Shaoyang Liu (2010)
10.1007/S13534-011-0009-8
Recent research trends in nanoscale electro-mechanical systems for bio-medical applications
Su Ho Chung (2011)
10.1021/la203752y
EMSA and single-molecule force spectroscopy study of interactions between Bacillus subtilis single-stranded DNA-binding protein and single-stranded DNA.
W. Zhang (2011)
Technology Assessment and Feasibility Study of High- Throughput Single Cell Force Spectroscopy By
He Cheng (2010)
Studying Biomolecular Structures and Their Interaction Using Atomic Force Microscopy
Subhadip Senapati (2015)
10.1007/978-981-13-1510-7_5
Atomic Force Microscopy: A Nanoscopic Application in Molecular and Cell Biology
Huaihong Cai (2018)
10.1002/ADMI.201800616
Single‐Crack‐Activated Ultrasensitive Impedance Strain Sensor
Jilong Ye (2018)
10.1021/BI800753X
AFM: a nanotool in membrane biology.
D. Müller (2008)
10.1073/pnas.0905384106
Immune synapse formation determines interaction forces between T cells and antigen-presenting cells measured by atomic force microscopy
B. H. Hosseini (2009)
10.1063/1.4774296
Relationship between disease-specific structures of amyloid fibrils and their mechanical properties
G. Yoon (2013)
10.1016/j.tibtech.2013.05.004
Proteins behaving badly: emerging technologies in profiling biopharmaceutical aggregation.
Zahra Hamrang (2013)
10.1021/la4042524
Nanoscale imaging and mechanical analysis of Fc receptor-mediated macrophage phagocytosis against cancer cells.
M. Li (2014)
10.3390/ijms21031066
The Clustering of mApoE Anti-Amyloidogenic Peptide on Nanoparticle Surface Does Not Alter Its Performance in Controlling Beta-Amyloid Aggregation
R. Corti (2020)
10.1039/c6cs00636a
Cellular uptake of nanoparticles: journey inside the cell.
Shahed Behzadi (2017)
10.1109/NEMS.2011.6017326
Imaging and measuring the protein distribution of lymphoma cells using atomic force microscopy
M. Li (2011)
10.1021/bi400913x
Single-molecule studies of bacterial protein translocation.
A. Kedrov (2013)
10.1038/nmeth0211-123
Five challenges to bringing single-molecule force spectroscopy into living cells
Y. Dufrêne (2011)
10.1002/adma.201002270
Recent trends in surface characterization and chemistry with high-resolution scanning force methods.
C. Barth (2011)
10.3390/ijms10094009
Experimental and Computational Characterization of Biological Liquid Crystals: A Review of Single-Molecule Bioassays
Kilho Eom (2009)
10.1016/j.nano.2011.10.004
Infection by Plasmodium changes shape and stiffness of hepatic cells.
P. Eaton (2012)
10.1007/978-1-4419-8411-1_8
Investigation of Protein–Protein Interactions in Cancer Targeted Therapy Using Nanorobots
M. Li (2013)
10.1115/IMECE2011-63478
Applicability Of Continuum Fracture Mechanics In Atomistic Systems
Shao-Huan Cheng (2011)
10.1038/ncomms3121
Direct measurement and modulation of single-molecule coordinative bonding forces in a transition metal complex.
X. Hao (2013)
Scanning Probe Investigations of the Surface Self-Assembly of Organothiols and Organosilanes Using Nanoscale Lithography
T. Tian (2013)
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