User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Force nanoscopy of cell mechanics and cell adhesion

Primary tabs

Dufrêne, Yves [UCL] Pelling, Andrew E. [Universiy of Ottawa]

Cells are constantly exposed to mechanical stimuli in their environment and have several evolved mechanisms to sense and respond to these cues. It is becoming increasingly recognized that many cell types, from bacteria to mammalian cells, possess a diverse set of proteins to translate mechanical cues into biochemical signalling and to mediate cell surface interactions such as cell adhesion. Moreover, the mechanical properties of cells are involved in regulating cell function as well as serving as indicators of disease states. Importantly, the recent development of biophysical tools and nanoscale methods has facilitated a deeper understanding of the role that physical forces play in modulating cell mechanics and cell adhesion. Here, we discuss how atomic force microscopy (AFM) has recently been used to investigate cell mechanics and cell adhesion at the single-cell and single-molecule levels. This knowledge is critical to our understanding of the molecular mechanisms that govern mechanosensing, mechanotransduction, and mechanoresponse in living cells. While pushing living cells with the AFM tip provides a means to quantify their mechanical properties and examine their response to nanoscale forces, pulling single surface proteins with a functionalized tip allows one to understand their role in sensing and adhesion. The combination of these nanoscale techniques with modern molecular biology approaches, genetic engineering and optical microscopies provides a powerful platform for understanding the sophisticated functions of the cell surface machinery, and its role in the onset and progression of complex diseases

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2013
Language Anglais
Journal information "Nanoscale" - Vol. 5, p. 4094–4104 (2013)
Peer reviewed yes
Publisher National Center for Nanoscience and Technology
issn 2040-3364
e-issn 2040-3372
Publication status Publié
Affiliations UCL - SST/ISV - Institut des sciences de la vie
UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
Links
  1. Bukoreshtliev Nickolay V., Haase Kristina, Pelling Andrew E., Mechanical cues in cellular signalling and communication, 10.1007/s00441-012-1531-4
  2. Janmey P. A., Miller R. T., Mechanisms of mechanical signaling in development and disease, 10.1242/jcs.071001
  3. Mammoto Akiko, Mammoto Tadanori, Ingber Donald E., Mechanosensitive mechanisms in transcriptional regulation, 10.1242/jcs.093005
  4. Vogel Viola, Sheetz Michael, Local force and geometry sensing regulate cell functions, 10.1038/nrm1890
  5. Schwartz M. A., CELL BIOLOGY: The Force Is with Us, 10.1126/science.1169414
  6. Wirtz Denis, Konstantopoulos Konstantinos, Searson Peter C., The physics of cancer: the role of physical interactions and mechanical forces in metastasis, 10.1038/nrc3080
  7. Busscher Henk J., van der Mei Henny C., How Do Bacteria Know They Are on a Surface and Regulate Their Response to an Adhering State?, 10.1371/journal.ppat.1002440
  8. Iscla Irene, Blount Paul, Sensing and Responding to Membrane Tension: The Bacterial MscL Channel as a Model System, 10.1016/j.bpj.2012.06.021
  9. Monshausen Gabriele B., Gilroy Simon, Feeling green: mechanosensing in plants, 10.1016/j.tcb.2009.02.005
  10. Brown André E.X., Discher Dennis E., Conformational Changes and Signaling in Cell and Matrix Physics, 10.1016/j.cub.2009.06.054
  11. Buxboim A., Ivanovska I. L., Discher D. E., Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in?, 10.1242/jcs.041186
  12. Schwarz Ulrich S., Gardel Margaret L., United we stand – integrating the actin cytoskeleton and cell–matrix adhesions in cellular mechanotransduction, 10.1242/jcs.093716
  13. Heinisch J. J., Lipke P. N., Beaussart A., El Kirat Chatel S., Dupres V., Alsteens D., Dufrene Y. F., Atomic force microscopy - looking at mechanosensors on the cell surface, 10.1242/jcs.106005
  14. Sukharev Sergei, Sachs Frederick, Molecular force transduction by ion channels – diversity and unifying principles, 10.1242/jcs.092353
  15. Kobayashi Takeshi, Sokabe Masahiro, Sensing substrate rigidity by mechanosensitive ion channels with stress fibers and focal adhesions, 10.1016/j.ceb.2010.08.023
  16. Rodicio Rosaura, Heinisch Jürgen J., Together we are strong-cell wall integrity sensors in yeasts, 10.1002/yea.1785
  17. Dupres Vincent, Alsteens David, Wilk Sabrina, Hansen Benjamin, Heinisch Jürgen J, Dufrêne Yves F, The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo, 10.1038/nchembio.220
  18. Domke J., Parak Wolfgang J., George Michael, Gaub Hermann E., Radmacher M., Mapping the mechanical pulse of single cardiomyocytes with the atomic force microscope, 10.1007/s002490050198
  19. Pelling A. E., Local Nanomechanical Motion of the Cell Wall of Saccharomyces cerevisiae, 10.1126/science.1097640
  20. Cuerrier Charles M., Benoit Martin, Guillemette Gaétan, Jr. Gobeil Fernand, Grandbois Michel, Real-time monitoring of angiotensin II-induced contractile response and cytoskeleton remodeling in individual cells by atomic force microscopy, 10.1007/s00424-008-0596-0
  21. Prass Marcus, Jacobson Ken, Mogilner Alex, Radmacher Manfred, Direct measurement of the lamellipodial protrusive force in a migrating cell, 10.1083/jcb.200601159
  22. Pelling Andrew E., Veraitch Farlan S., Pui-Kei Chu Carol, Nicholls Brian M., Hemsley Alexandra L., Mason Chris, Horton Michael A., Mapping correlated membrane pulsations and fluctuations in human cells, 10.1002/jmr.832
  23. Eyckmans Jeroen, Boudou Thomas, Yu Xiang, Chen Christopher S., A Hitchhiker's Guide to Mechanobiology, 10.1016/j.devcel.2011.06.015
  24. Engler Adam J., Griffin Maureen A., Sen Shamik, Bönnemann Carsten G., Sweeney H. Lee, Discher Dennis E., Myotubes differentiate optimally on substrates with tissue-like stiffness : pathological implications for soft or stiff microenvironments, 10.1083/jcb.200405004
  25. Engler Adam J., Sen Shamik, Sweeney H. Lee, Discher Dennis E., Matrix Elasticity Directs Stem Cell Lineage Specification, 10.1016/j.cell.2006.06.044
  26. Paszek Matthew J., Zahir Nastaran, Johnson Kandice R., Lakins Johnathon N., Rozenberg Gabriela I., Gefen Amit, Reinhart-King Cynthia A., Margulies Susan S., Dembo Micah, Boettiger David, Hammer Daniel A., Weaver Valerie M., Tensional homeostasis and the malignant phenotype, 10.1016/j.ccr.2005.08.010
  27. Hogan Catherine, Dupré-Crochet Sophie, Norman Mark, Kajita Mihoko, Zimmermann Carola, Pelling Andrew E., Piddini Eugenia, Baena-López Luis Alberto, Vincent Jean-Paul, Itoh Yoshifumi, Hosoya Hiroshi, Pichaud Franck, Fujita Yasuyuki, Characterization of the interface between normal and transformed epithelial cells, 10.1038/ncb1853
  28. Pelling Andrew E., Veraitch Farlan S., Chu Carol Pui-Kei, Mason Chris, Horton Michael A., Mechanical dynamics of single cells during early apoptosis, 10.1002/cm.20391
  29. Guvendiren Murat, Burdick Jason A., Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics, 10.1038/ncomms1792
  30. Guolla L., Bertrand M., Haase K., Pelling A. E., Force transduction and strain dynamics in actin stress fibres in response to nanonewton forces, 10.1242/jcs.088302
  31. Maniotis A. J., Chen C. S., Ingber D. E., Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure, 10.1073/pnas.94.3.849
  32. Na S., Collin O., Chowdhury F., Tay B., Ouyang M., Wang Y., Wang N., Rapid signal transduction in living cells is a unique feature of mechanotransduction, 10.1073/pnas.0711704105
  33. Silberberg Yaron R., Pelling Andrew E., Yakubov Gleb E., Crum William R., Hawkes David J., Horton Mike A., Mitochondrial displacements in response to nanomechanical forces, 10.1002/jmr.868
  34. Charras Guillaume T., Horton Mike A., Single Cell Mechanotransduction and Its Modulation Analyzed by Atomic Force Microscope Indentation, 10.1016/s0006-3495(02)75638-5
  35. Formigli L., Sphingosine 1-phosphate induces cytoskeletal reorganization in C2C12 myoblasts: physiological relevance for stress fibres in the modulation of ion current through stretch-activated channels, 10.1242/jcs.01695
  36. Wang Jiaxu, Su Ming, Fan Jennie, Seth Arun, McCulloch Christopher A., Transcriptional Regulation of a Contractile Gene by Mechanical Forces Applied through Integrins in Osteoblasts, 10.1074/jbc.m203130200
  37. Kunda Patricia, Pelling Andrew E., Liu Tao, Baum Buzz, Moesin Controls Cortical Rigidity, Cell Rounding, and Spindle Morphogenesis during Mitosis, 10.1016/j.cub.2007.12.051
  38. Matzke Rainer, Jacobson Ken, Radmacher Manfred, 10.1038/35078583
  39. Stewart Martin P., Helenius Jonne, Toyoda Yusuke, Ramanathan Subramanian P., Muller Daniel J., Hyman Anthony A., Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding, 10.1038/nature09642
  40. Pelling Andrew E., Horton Michael A., An historical perspective on cell mechanics, 10.1007/s00424-007-0405-1
  41. Bao G., Suresh S., Cell and molecular mechanics of biological materials, 10.1038/nmat1001
  42. Müller Daniel J., Dufrêne Yves F., Atomic force microscopy: a nanoscopic window on the cell surface, 10.1016/j.tcb.2011.04.008
  43. Lab M. J., Bhargava A., Wright P. T., Gorelik J., The scanning ion conductance microscope for cellular physiology, 10.1152/ajpheart.00499.2012
  44. Deniz A. A, Mukhopadhyay S., Lemke E. A, Single-molecule biophysics: at the interface of biology, physics and chemistry, 10.1098/rsif.2007.1021
  45. Guck Jochen, Ananthakrishnan Revathi, Mahmood Hamid, Moon Tess J., Cunningham C. Casey, Käs Josef, The Optical Stretcher: A Novel Laser Tool to Micromanipulate Cells, 10.1016/s0006-3495(01)75740-2
  46. Kim Deok-Ho, Wong Pak Kin, Park Jungyul, Levchenko Andre, Sun Yu, Microengineered Platforms for Cell Mechanobiology, 10.1146/annurev-bioeng-061008-124915
  47. Okabe Kohki, Inada Noriko, Gota Chie, Harada Yoshie, Funatsu Takashi, Uchiyama Seiichi, Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy, 10.1038/ncomms1714
  48. Meng F., Sachs F., Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor, 10.1242/jcs.071928
  49. Lippincott-Schwartz Jennifer, Patterson George H., Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging, 10.1016/j.tcb.2009.09.003
  50. Gerber Christoph, Lang Hans Peter, How the doors to the nanoworld were opened, 10.1038/nnano.2006.70
  51. Müller Daniel J., Dufrêne Yves F., Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology, 10.1038/nnano.2008.100
  52. Kodera Noriyuki, Yamamoto Daisuke, Ishikawa Ryoki, Ando Toshio, Video imaging of walking myosin V by high-speed atomic force microscopy, 10.1038/nature09450
  53. Leung Carl, Bestembayeva Aizhan, Thorogate Richard, Stinson Jake, Pyne Alice, Marcovich Christian, Yang Jinling, Drechsler Ute, Despont Michel, Jankowski Tilo, Tschöpe Martin, Hoogenboom Bart W., Atomic Force Microscopy with Nanoscale Cantilevers Resolves Different Structural Conformations of the DNA Double Helix, 10.1021/nl301857p
  54. Martinez-Martin David, Carrasco Carolina, Hernando-Perez Mercedes, de Pablo Pedro J., Gomez-Herrero Julio, Perez Rebeca, Mateu Mauricio G., Carrascosa Jose L., Kiracofe Daniel, Melcher John, Raman Arvind, Resolving Structure and Mechanical Properties at the Nanoscale of Viruses with Frequency Modulation Atomic Force Microscopy, 10.1371/journal.pone.0030204
  55. Polyakov Pavel, Soussen Charles, Duan Junbo, Duval Jérôme F. L., Brie David, Francius Grégory, Automated Force Volume Image Processing for Biological Samples, 10.1371/journal.pone.0018887
  56. El-Kirat-Chatel, ACS Nano, 6, 10792 (2012)
  57. Müller Daniel J, Helenius Jonne, Alsteens David, Dufrêne Yves F, Force probing surfaces of living cells to molecular resolution, 10.1038/nchembio.181
  58. Lévy R, Maaloum M, Measuring the spring constant of atomic force microscope cantilevers: thermal fluctuations and other methods, 10.1088/0957-4484/13/1/307
  59. Janmey Paul A., McCulloch Christopher A., Cell Mechanics: Integrating Cell Responses to Mechanical Stimuli, 10.1146/annurev.bioeng.9.060906.151927
  60. Pelling A. E., Li Y., Shi W., Gimzewski J. K., Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy, 10.1073/pnas.0501207102
  61. ROTSCH C, AFM IMAGING AND ELASTICITY MEASUREMENTS ON LIVING RAT LIVER MACROPHAGES, 10.1006/cbir.1997.0213
  62. Rotsch C., Jacobson K., Radmacher M., Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy, 10.1073/pnas.96.3.921
  63. Rotsch Christian, Radmacher Manfred, Drug-Induced Changes of Cytoskeletal Structure and Mechanics in Fibroblasts: An Atomic Force Microscopy Study, 10.1016/s0006-3495(00)76614-8
  64. Harris Andrew R, Charras G T, Experimental validation of atomic force microscopy-based cell elasticity measurements, 10.1088/0957-4484/22/34/345102
  65. Lehenkari P.P, Charras G.T, Nykänen A, Horton M.A, Adapting atomic force microscopy for cell biology, 10.1016/s0304-3991(99)00138-2
  66. Hinterdorfer Peter, Dufrêne Yves F, Detection and localization of single molecular recognition events using atomic force microscopy, 10.1038/nmeth871
  67. Puchner Elias M, Gaub Hermann E, Force and function: probing proteins with AFM-based force spectroscopy, 10.1016/j.sbi.2009.09.005
  68. Karácsony Orsolya, Akhremitchev Boris B., On the Detection of Single Bond Ruptures in Dynamic Force Spectroscopy by AFM, 10.1021/la202530j
  69. Benoit Martin, Gabriel Daniela, Gerisch Günther, Gaub Hermann E., 10.1038/35014000
  70. Franz C. M., Taubenberger A., Puech P.-H., Muller D. J., Studying Integrin-Mediated Cell Adhesion at the Single-Molecule Level Using AFM Force Spectroscopy, 10.1126/stke.4062007pl5
  71. Friedrichs Jens, Helenius Jonne, Muller Daniel J, Quantifying cellular adhesion to extracellular matrix components by single-cell force spectroscopy, 10.1038/nprot.2010.89
  72. Helenius J., Heisenberg C.-P., Gaub H. E., Muller D. J., Single-cell force spectroscopy, 10.1242/jcs.030999
  73. Hoh, J. Cell Sci., 107, 1105 (1994)
  74. Cross Sarah E., Jin Yu-Sheng, Rao Jianyu, Gimzewski James K., Nanomechanical analysis of cells from cancer patients, 10.1038/nnano.2007.388
  75. Iyer S., Gaikwad R. M., Subba-Rao V., Woodworth C. D., Sokolov Igor, Atomic force microscopy detects differences in the surface brush of normal and cancerous cells, 10.1038/nnano.2009.77
  76. Plodinec Marija, Loparic Marko, Monnier Christophe A., Obermann Ellen C., Zanetti-Dallenbach Rosanna, Oertle Philipp, Hyotyla Janne T., Aebi Ueli, Bentires-Alj Mohamed, Lim Roderick Y. H., Schoenenberger Cora-Ann, The nanomechanical signature of breast cancer, 10.1038/nnano.2012.167
  77. Kajita M., Hogan C., Harris A. R., Dupre-Crochet S., Itasaki N., Kawakami K., Charras G., Tada M., Fujita Y., Interaction with surrounding normal epithelial cells influences signalling pathways and behaviour of Src-transformed cells, 10.1242/jcs.057976
  78. Silberberg Yaron R, Yakubov Gleb E, Horton Michael A, Pelling Andrew E, Cell nanomechanics and focal adhesions are regulated by retinol and conjugated linoleic acid in a dose-dependent manner, 10.1088/0957-4484/20/28/285103
  79. Wu H. W., Kuhn T., Moy V. T., Mechanical properties of L929 cells measured by atomic force microscopy: Effects of anticytoskeletal drugs and membrane crosslinking, 10.1002/sca.1998.4950200504
  80. KASSIES R., VAN DER WERF K. O., LENFERINK A., HUNTER C. N., OLSEN J. D., SUBRAMANIAM V., OTTO C., Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology, 10.1111/j.0022-2720.2005.01428.x
  81. Haupt B.J., Pelling A.E., Horton M.A., Integrated Confocal and Scanning Probe Microscopy for Biomedical Research, 10.1100/tsw.2006.269
  82. Hemsley, Cell Health Cytoskeleton, 3, 23 (2011)
  83. Wang Jiaxu, Fan Jennie, Laschinger Carol, Arora Pamela D., Kapus Andras, Seth Arun, McCulloch Christopher A., Smooth Muscle Actin Determines Mechanical Force-induced p38 Activation, 10.1074/jbc.m410819200
  84. Ng C. P., Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro, 10.1242/jcs.02605
  85. Rief M., Reversible Unfolding of Individual Titin Immunoglobulin Domains by AFM, 10.1126/science.276.5315.1109
  86. Fernandez Julio M., Oberhauser Andres F., Marszalek Piotr E., Erickson Harold P., 10.1038/30270
  87. Oesterhelt F., Unfolding Pathways of Individual Bacteriorhodopsins, 10.1126/science.288.5463.143
  88. Galera-Prat Albert, Gómez-Sicilia Angel, Oberhauser Andres F., Cieplak Marek, Carrión-Vázquez Mariano, Understanding biology by stretching proteins: recent progress, 10.1016/j.sbi.2010.01.003
  89. Li Hongbin, Cao Yi, Protein Mechanics: From Single Molecules to Functional Biomaterials, 10.1021/ar100057a
  90. Dufrêne Yves F, Evans Evan, Engel Andreas, Helenius Jonne, Gaub Hermann E, Müller Daniel J, Five challenges to bringing single-molecule force spectroscopy into living cells, 10.1038/nmeth0211-123
  91. Heinisch Jürgen J, Dupres Vincent, Alsteens David, Dufrêne Yves F, Measurement of the mechanical behavior of yeast membrane sensors using single-molecule atomic force microscopy, 10.1038/nprot.2010.19
  92. Alsteens David, Dupres Vincent, Klotz Stephen A., Gaur Nand K., Lipke Peter N., Dufrêne Yves F., Unfolding Individual Als5p Adhesion Proteins on Live Cells, 10.1021/nn900078p
  93. Alsteens David, Ramsook Caleen B., Lipke Peter N., Dufrêne Yves F., Unzipping a Functional Microbial Amyloid, 10.1021/nn3025699
  94. Worth D. C., Parsons M., Advances in imaging cell-matrix adhesions, 10.1242/jcs.064485
  95. Chtcheglova Lilia A., Waschke Jens, Wildling Linda, Drenckhahn Detlev, Hinterdorfer Peter, Nano-Scale Dynamic Recognition Imaging on Vascular Endothelial Cells, 10.1529/biophysj.107.109751
  96. Kim Hyonchol, Arakawa Hideo, Hatae Noriyuki, Sugimoto Yukihiko, Matsumoto Osamu, Osada Toshiya, Ichikawa Atsushi, Ikai Atsushi, Quantification of the number of EP3 receptors on a living CHO cell surface by the AFM, 10.1016/j.ultramic.2005.12.007
  97. Roduit Charles, van der Goot F. Gisou, De Los Rios Paolo, Yersin Alexandre, Steiner Pascal, Dietler Giovanni, Catsicas Stefan, Lafont Frank, Kasas Sandor, Elastic Membrane Heterogeneity of Living Cells Revealed by Stiff Nanoscale Membrane Domains, 10.1529/biophysj.107.112862
  98. Beaussart, ACS Nano, 6, 10950 (2012)
  99. Heinisch Jürgen J., Dupres Vincent, Wilk Sabrina, Jendretzki Arne, Dufrêne Yves F., Single-Molecule Atomic Force Microscopy Reveals Clustering of the Yeast Plasma-Membrane Sensor Wsc1, 10.1371/journal.pone.0011104
  100. Alsteens D., Garcia M. C., Lipke P. N., Dufrene Y. F., Force-induced formation and propagation of adhesion nanodomains in living fungal cells, 10.1073/pnas.1013893107
  101. Shibata Mikihiro, Yamashita Hayato, Uchihashi Takayuki, Kandori Hideki, Ando Toshio, High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin, 10.1038/nnano.2010.7
  102. Medalsy Izhar, Hensen Ulf, Muller Daniel J., Imaging and Quantifying Chemical and Physical Properties of Native Proteins at Molecular Resolution by Force-Volume AFM, 10.1002/anie.201103991
  103. Alsteens David, Dupres Vincent, Yunus Sami, Latgé Jean-Paul, Heinisch Jürgen J., Dufrêne Yves F., High-Resolution Imaging of Chemical and Biological Sites on Living Cells Using Peak Force Tapping Atomic Force Microscopy, 10.1021/la303891j
  104. Sharma Shivani, Santiskulvong Chintda, Bentolila Laurent A., Rao JianYu, Dorigo Oliver, Gimzewski James K., Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells, 10.1016/j.nano.2011.09.015
  105. Ivanov Ivan E., Boyd Chelsea D., Newell Peter D., Schwartz Mary E., Turnbull Lynne, Johnson Michael S., Whitchurch Cynthia B., O'Toole George A., Camesano Terri A., Atomic force and super-resolution microscopy support a role for LapA as a cell-surface biofilm adhesin of Pseudomonas fluorescens, 10.1016/j.resmic.2012.10.001
  106. Hardie R. C., Franze K., Photomechanical Responses in Drosophila Photoreceptors, 10.1126/science.1222376
  107. Diz-Muñoz Alba, Krieg Michael, Bergert Martin, Ibarlucea-Benitez Itziar, Muller Daniel J., Paluch Ewa, Heisenberg Carl-Philipp, Control of Directed Cell Migration In Vivo by Membrane-to-Cortex Attachment, 10.1371/journal.pbio.1000544
Bibliographic reference Dufrêne, Yves ; Pelling, Andrew E.. Force nanoscopy of cell mechanics and cell adhesion. In: Nanoscale, Vol. 5, p. 4094–4104 (2013)
Permanent URL http://hdl.handle.net/2078.1/128530