Mapping heterogeneity of cellular mechanics by multi-harmonic atomic force microscopy

0
8


  • 1.

    Nelson, C. M. et al. Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. USA 102, 11594–11599 (2005).

  • 2.

    Wang, N., Tytell, J. D. & Ingber, D. E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75–82 (2009).

  • 3.

    Rotsch, C., Jacobson, K. & Radmacher, M. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl. Acad. Sci. USA 96, 921–926 (1999).

  • 4.

    Lange, J. R. & Fabry, B. Cell and tissue mechanics in cell migration. Exp. Cell Res. 319, 2418–2423 (2013).

  • 5.

    Friedl, P., Wolf, K. & Lammerding, J. Nuclear mechanics during cell migration. Curr. Opin. Cell Biol. 23, 55–64 (2011).

  • 6.

    Franze, K., Janmey, P. A. & Guck, J. Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15, 227–251 (2013).

  • 7.

    Kumar, S. & Weaver, V. M. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113–127 (2009).

  • 8.

    Wirtz, D., Konstantopoulos, K. & Searson, P. C. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11, 512–522 (2011).

  • 9.

    Suresh, S. Biomechanics and biophysics of cancer cells. Acta Mater. 55, 3989–4014 (2007).

  • 10.

    Rotsch, C. & Radmacher, M. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys. J. 78, 520–535 (2000).

  • 11.

    Efremov, Y. M. et al. Distinct impact of targeted actin cytoskeleton reorganization on mechanical properties of normal and malignant cells. Biochim. Biophys. Acta 1853, 3117–3125 (2015).

  • 12.

    Grady, M. E., Composto, R. J. & Eckmann, D. M. in Mechanics of Biological Systems and Materials (eds. Barthelat, F., Zavattieri, P., Korach, C. S., Prorok, B. C. & Grande-Allen, K. J.) 6, 169–177 (Springer, New York, 2017).

  • 13.

    Cross, S. E., Jin, Y. S., Rao, J. & Gimzewski, J. K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2, 780–783 (2007).

  • 14.

    Lekka, M. et al. Cancer cell recognition–mechanical phenotype. Micron 43, 1259–1266 (2012).

  • 15.

    van Zwieten, R. W. et al. Assessing dystrophies and other muscle diseases at the nanometer scale by atomic force microscopy. Nanomedicine 9, 393–406 (2014).

  • 16.

    Burridge, K. & Guilluy, C. Focal adhesions, stress fibers and mechanical tension. Exp. Cell Res. 343, 14–20 (2016).

  • 17.

    Ingber, D. E., Wang, N. & Stamenovic, D. Tensegrity, cellular biophysics, and the mechanics of living systems. Rep. Prog. Phys. 77, 046603 (2014).

  • 18.

    Plotnikov, S. V., Pasapera, A. M., Sabass, B. & Waterman, C. M. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513–1527 (2012).

  • 19.

    Park, C. Y. et al. Mapping the cytoskeletal prestress. Am. J. Physiol. Cell Physiol. 298, C1245–C1252 (2010).

  • 20.

    Hochmuth, R. M. Micropipette aspiration of living cells. J. Biomech. 33, 15–22 (2000).

  • 21.

    Desprat, N., Richert, A., Simeon, J. & Asnacios, A. Creep function of a single living cell. Biophys. J. 88, 2224–2233 (2005).

  • 22.

    Caille, N., Thoumine, O., Tardy, Y. & Meister, J. J. Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech. 35, 177–187 (2002).

  • 23.

    Ayala, Y. A. et al. Rheological properties of cells measured by optical tweezers. BMC Biophys. 9, 5 (2016).

  • 24.

    Wei, M.-T. et al. A comparative study of living cell micromechanical properties by oscillatory optical tweezers. Opt. Express 16, 8594–8603 (2008).

  • 25.

    Hu, S. et al. Mechanical anisotropy of adherent cells probed by a three-dimensional magnetic twisting device. Am. J. Physiol. Cell Physiol. 287, C1184–C1191 (2004).

  • 26.

    Hoffman, B. D., Massiera, G., Van Citters, K. M. & Crocker, J. C. The consensus mechanics of cultured mammalian cells. Proc. Natl. Acad. Sci. USA 103, 10259–10264 (2006).

  • 27.

    Haga, H. et al. Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton. Ultramicroscopy 82, 253–258 (2000).

  • 28.

    Cartagena-Rivera, A. X., Wang, W.-H., Geahlen, R. L. & Raman, A. Fast, multi-frequency, and quantitative nanomechanical mapping of live cells using the atomic force microscope. Sci. Rep. 5, 11692 (2015).

  • 29.

    A-Hassan, E. et al. Relative microelastic mapping of living cells by atomic force microscopy. Biophys. J. 74, 1564–1578 (1998).

  • 30.

    Kuznetsova, T. G., Starodubtseva, M. N., Yegorenkov, N. I., Chizhik, S. A. & Zhdanov, R. I. Atomic force microscopy probing of cell elasticity. Micron 38, 824–833 (2007).

  • 31.

    Gavara, N. A beginner’s guide to atomic force microscopy probing for cell mechanics. Microsc. Res. Tech. 1–10 (2016).

  • 32.

    Efremov, Y. M., Wang, W.-H., Hardy, S. D., Geahlen, R. L. & Raman, A. Measuring nanoscale viscoelastic parameters of cells directly from AFM force-displacement curves. Sci. Rep. 7, 1541 (2017).

  • 33.

    Rico, F. et al. Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Phys. Rev. E 72, 21914 (2005).

  • 34.

    Radmacher, M. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 68, 67–90 (2002).

  • 35.

    Garcia, P. D., Guerrero, C. R. & Garcia, R. Time-resolved nanomechanics of a single cell under the depolymerization of the cytoskeleton. Nanoscale 9, 12051–12059 (2017).

  • 36.

    Brückner, B. R., Nöding, H. & Janshoff, A. Viscoelastic properties of confluent MDCK II cells obtained from force cycle experiments. Biophys. J. 112, 724–735 (2017).

  • 37.

    Raman, A. et al. Mapping nanomechanical properties of live cells using multi-harmonic atomic force microscopy. Nat. Nanotechnol. 6, 809–814 (2011).

  • 38.

    Sahin, O. et al. High-resolution imaging of elastic properties using harmonic cantilevers. Sens. Actuators A Phys. 114, 183–190 (2004).

  • 39.

    van Noort, S. J. T., Willemsen, O. H., van der Werf, K. O., de Grooth, B. G. & Greve, J. Mapping electrostatic forces using higher harmonics tapping mode atomic force microscopy in liquid. Langmuir 15, 7101–7107 (1999).

  • 40.

    Dufrêne, Y. F. et al. Imaging modes of atomic force microscopy for application in molecular and cell biology. Nat. Nanotechnol. 12, 295–307 (2017).

  • 41.

    Chyasnavichyus, M., Young, S. L. & Tsukruk, V. V. Recent advances in micromechanical characterization of polymer, biomaterial, and cell surfaces with atomic force microscopy. Jpn. J. Appl. Phys. 54, 08LA02 (2015).

  • 42.

    Tung, R. C., Jana, A. & Raman, A. Hydrodynamic loading of microcantilevers oscillating near rigid walls. J. Appl. Phys. 104, 114905 (2008).

  • 43.

    Cartagena, A. & Raman, A. Local viscoelastic properties of live cells investigated using dynamic and quasi-static atomic force microscopy methods. Biophys. J. 106, 1033–1043 (2014).

  • 44.

    Cartagena, A., Hernando-Pérez, M., Carrascosa, J. L., de Pablo, P. J. & Raman, A. Mapping in vitro local material properties of intact and disrupted virions at high resolution using multi-harmonic atomic force microscopy. Nanoscale 5, 4729–4736 (2013).

  • 45.

    Melcher, J. et al. Origins of phase contrast in the atomic force microscope in liquids. Proc. Natl. Acad. Sci. USA 106, 13655–13660 (2009).

  • 46.

    Xu, X., Melcher, J., Basak, S., Reifenberger, R. & Raman, A. Compositional contrast of biological materials in liquids using the momentary excitation of higher eigenmodes in dynamic atomic force microscopy. Phys. Rev. Lett. 102, 060801 (2009).

  • 47.

    Hertz, H. Über die Berührung Fester Elastischer Körper. J. reine u. angew. Math. 92, 156–171 (1881).

  • 48.

    Sneddon, I. N. The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. Int. J. Eng. Sci. 3, 47–57 (1965).

  • 49.

    Dimitriadis, E. K., Horkay, F., Maresca, J., Kachar, B. & Chadwick, R. S. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82, 2798–2810 (2002).

  • 50.

    Gavara, N. & Chadwick, R. S. Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips. Nat. Nanotechnol. 7, 733–736 (2012).

  • 51.

    Krisenko, M. O., Cartagena, A., Raman, A. & Geahlen, R. L. Nanomechanical property maps of breast cancer cells as determined by multiharmonic atomic force microscopy reveal Syk-dependent changes in microtubule stability mediated by MAP1B. Biochemistry 54, 60–68 (2015).

  • 52.

    Kronlage, C., Schäfer-Herte, M., Böning, D., Oberleithner, H. & Fels, J. Feeling for filaments: quantification of the cortical actin web in live vascular endothelium. Biophys. J. 109, 687–698 (2015).

  • 53.

    Smolyakov, G., Formosa-Dague, C., Severac, C., Duval, R. E. & Dague, E. High speed indentation measures by FV, QI and QNM introduce a new understanding of bionanomechanical experiments. Micron 85, 8–14 (2016).

  • 54.

    Schillers, H., Medalsy, I., Hu, S., Slade, A. L. & Shaw, J. E. PeakForce tapping resolves individual microvilli on living cells. J. Mol. Recognit. 29, 95–101 (2016).

  • 55.

    Calzado-Martín, A., Encinar, M., Tamayo, J., Calleja, M. & San Paulo, A. Effect of actin organization on the stiffness of living breast cancer cells revealed by peak-force modulation atomic force microscopy. ACS Nano (2016). https://doi.org/10.1021/acsnano.5b07162.

  • 56.

    Ando, T. Directly watching biomolecules in action by high-speed atomic force microscopy. Biophys. Rev. 9, 421–429 (2017).

  • 57.

    Vogel, V. & Sheetz, M. P. Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr. Opin. Cell Biol. 21, 38–46 (2009).

  • 58.

    Xu, X. & Raman, A. Comparative dynamics of magnetically, acoustically, and Brownian motion driven microcantilevers in liquids. J. Appl. Phys. 102, 034303 (2007).

  • 59.

    Enders, O., Korte, F. & Kolb, H.-A. Lorentz-force-induced excitation of cantilevers for oscillation-mode scanning probe microscopy. Surf. Interface Anal. 36, 119–123 (2004).

  • 60.

    Kiracofe, D., Kobayashi, K., Labuda, A., Raman, A. & Yamada, H. High efficiency laser photothermal excitation of microcantilever vibrations in air and liquids. Rev. Sci. Instrum. 82, 013702 (2011).

  • 61.

    Labuda, A. et al. Comparison of photothermal and piezoacoustic excitation methods for frequency and phase modulation atomic force microscopy in liquid environments. AIP Adv. 1, 022136 (2011).

  • 62.

    Rabe, U. & Arnold, W. Acoustic microscopy by atomic force microscopy. Appl. Phys. Lett. 64, 1493–1495 (1994).

  • 63.

    Schäffer, T. E., Cleveland, J. P., Ohnesorge, F., Walters, D. A. & Hansma, P. K. Studies of vibrating atomic force microscope cantilevers in liquid. J. Applied Physics 80, 3622 (2012).

  • 64.

    Kiracofe, D. & Raman, A. Quantitative force and dissipation measurements in liquids using piezo-excited atomic force microscopy: a unifying theory. Nanotechnology 22, 485502 (2011).

  • 65.

    Florin, E.-L., Radmacher, M., Fleck, B. & Gaub, H. E. Atomic force microscope with magnetic force modulation. Rev. Sci. Instrum. 65, 639 (1994).

  • 66.

    Han, W., Lindsay, S. M. & Jing, T. A magnetically driven oscillating probe microscope for operation in liquids. Appl. Phys. Lett. 69, 4111–4113 (1996).

  • 67.

    Ge, G. et al. MAC mode atomic force microscopy studies of living samples, ranging from cells to fresh tissue. Ultramicroscopy 107, 299–307 (2007).

  • 68.

    Wang, A., Butte, M. J., Wang, A. & Butte, M. J. Customized atomic force microscopy probe by focused-ion-beam-assisted tip transfer. Appl. Phys. Lett. 105, 053101 (2015).

  • 69.

    Nagao, E. & Dvorak, J. A. An integrated approach to the study of living cells by atomic force microscopy. J. Microsc. 191, 8–19 (1998).

  • 70.

    Garcia, R. & Herruzo, E. T. The emergence of multifrequency force microscopy. Nat. Nanotechnol. 7, 217–226 (2012).

  • 71.

    Garcia, R. & Proksch, R. Nanomechanical mapping of soft matter by bimodal force microscopy. Eur. Polym. J. 49, 1897–1906 (2013).

  • 72.

    Solares, S. D. & Chawla, G. Frequency response of higher cantilever eigenmodes in bimodal and trimodal tapping mode atomic force microscopy. Meas. Sci. Technol. 21, 125502 (2010).

  • 73.

    Balland, M. et al. Power laws in microrheology experiments on living cells: comparative analysis and modeling. Phys. Rev. E 74, 021911 (2006).

  • 74.

    Alcaraz, J. et al. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 84, 2071–2079 (2003).

  • 75.

    Rigato, A., Miyagi, A., Scheuring, S. & Rico, F. High-frequency microrheology reveals cytoskeleton dynamics in living cells. Nat. Phys. (2017). https://doi.org/10.1038/nphys4104.

  • 76.

    Kollmannsberger, P. & Fabry, B. Linear and nonlinear rheology of living cells. Annu. Rev. Mater. Res. 41, 75–97 (2011).

  • 77.

    Jonas, O. & Duschl, C. Force propagation and force generation in cells. Cytoskeleton 67, 555–563 (2010).

  • 78.

    Silberberg, Y. R. et al. Mitochondrial displacements in response to nanomechanical forces. J. Mol. Recognit. 21, 30–36 (2008).

  • 79.

    Krause, M., te Riet, J. & Wolf, K. Probing the compressibility of tumor cell nuclei by combined atomic force–confocal microscopy. Phys. Biol. 10, 065002 (2013).

  • 80.

    Rosenbluth, M. J., Crow, A., Shaevitz, J. W. & Fletcher, D. A. Slow stress propagation in adherent cells. Biophys. J. 95, 6052–6059 (2008).

  • 81.

    Lim, S.-M., Trzeciakowski, J. P., Sreenivasappa, H., Dangott, L. J. & Trache, A. RhoA-induced cytoskeletal tension controls adaptive cellular remodeling to mechanical signaling. Integr. Biol. 4, 615 (2012).

  • 82.

    Melzak, Ka & Toca-Herrera, J. L. Atomic force microscopy and cells: indentation profiles around the AFM tip, cell shape changes, and other examples of experimental factors affecting modeling. Microsc. Res. Tech. 78, 626–632 (2015).

  • 83.

    Trache, A. & Lim, S.-M. Integrated microscopy for real-time imaging of mechanotransduction studies in live cells. J. Biomed. Opt. 14, 034024 (2009).

  • 84.

    Staunton, J. R., Doss, B. L., Lindsay, S. & Ros, R. Correlating confocal microscopy and atomic force indentation reveals metastatic cancer cells stiffen during invasion into collagen I matrices. Sci. Rep. 6, 19686 (2016).

  • 85.

    Cascione, M., de Matteis, V., Rinaldi, R. & Leporatti, S. Atomic force microscopy combined with optical microscopy for cells investigation. Microsc. Res. Tech. 80, 109–123 (2017).

  • 86.

    Charras, G. T. & Horton, M. A. Determination of cellular strains by combined atomic force microscopy and finite element modeling. Biophys. J. 83, 858–879 (2002).

  • 87.

    Jonkman, J. & Brown, C. M. Any way you slice it-a comparison of confocal microscopy techniques. J. Biomol. Tech. 26, 54–65 (2015).

  • 88.

    Lulevich, V., Shih, Y. P., Lo, S. H. & Liu, G. Cell tracing dyes significantly change single cell mechanics. J. Phys. Chem. B 113, 6511–6519 (2009).

  • 89.

    Sliogeryte, K. et al. Differential effects of LifeAct-GFP and actin-GFP on cell mechanics assessed using micropipette aspiration. J. Biomech. 49, 310–317 (2016).

  • 90.

    Lee, A. C., Decourt, B. & Suter, D. Neuronal cell cultures from Aplysia for high-resolution imaging of growth cones. J. Vis. Exp. (2008). https://doi.org/10.3791/662.

  • 91.

    Suter, D. M. in Cell Migration. Methods in Molecular Biology (Methods and Protocols) (eds. Wells, C. & Parsons, M.) 65–86 (Humana Press, New York, 2011).

  • 92.

    Lukinavičius, G. et al. Fluorogenic probes for live-cell imaging of the cytoskeleton. Nat. Methods 11, 731–3 (2014).

  • 93.

    Sader, J. E. et al. A virtual instrument to standardise the calibration of atomic force microscope cantilevers. Rev. Sci. Instrum. 87, 093711 (2016).

  • 94.

    Schillers, H. et al. Standardized nanomechanical atomic force microscopy procedure (SNAP) for measuring soft and biological samples. Sci. Rep. 7, 5117 (2017).

  • 95.

    Hernando-Pérez, M. et al. Quantitative nanoscale electrostatics of viruses. Nanoscale 7, 17289–17298 (2015).

  • 96.

    Xiong, Y., Lee, A. C., Suter, D. M. & Lee, G. U. Topography and nanomechanics of live neuronal growth cones analyzed by atomic force microscopy. Biophys. J. 96, 5060–5072 (2009).

  • 97.

    Gallet, C. et al. Tyrosine phosphorylation of cortactin associated with Syk accompanies thromboxane analogue-induced platelet shape change. J. Biol. Chem. 274, 23610–23616 (1999).

  • 98.

    Le Roux, D. et al. Syk-dependent actin dynamics regulate endocytic trafficking and processing of antigens internalized through the B-cell receptor. Mol. Biol. Cell 18, 3451–3462 (2007).

  • 99.

    Braet, F., Rotsch, C., Wisse, E. & Radmacher, M. Comparison of fixed and living liver endothelial cells by atomic force microscopy. Appl. Phys. A Mater. Sci. Process. 66, 575–578 (1998).



  • Source link

    LEAVE A REPLY

    Please enter your comment!
    Please enter your name here