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Measuring the Elastic Properties of Living Cells

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First Online:
Part of the Methods in Molecular Biology book series (MIMB, volume 1886)

Abstract

Cell’s elasticity is an integrative parameter summarizing the biophysical outcome of many known and unknown cellular processes. This includes intracellular signaling, cytoskeletal activity, changes of cell volume and morphology, and many others. Not only intracellular processes defines a cell’s elasticity but also environmental factors like their biochemical and biophysical surrounding. Therefore, cell mechanics represents a comprehensive variable of life. A cell in its standard conditions shows variabilities of biochemical and biophysical processes resulting in a certain range of cell’s elasticity. Changes of the standard conditions, endogenously or exogenously induced, are frequently paralleled by changes of cell elasticity. Therefore cell elasticity could serve as parameter to characterize different states of a cell. Atomic force microscopy (AFM) combines high spatial resolution with very high force sensitivity and allows investigating mechanical properties of living cells under physiological conditions. However, elastic moduli reported in the literature showed a large variability, sometimes by an order of magnitude (or even more) for the same cell type assessed in different labs. Clearly, a prerequisite for the use of cell elasticity to describe the actual cell status is a standardized procedure that allows obtaining comparable values of a cell independent from the instrument, from the lab and operator. Biologically derived variations of elasticity could not be reduced due to the nature of living cells but technically and methodologically derived variations could be minimized by a standardized procedure.

This chapter provides a Standardized Nanomechanical AFM Procedure (SNAP) that reduces strongly the variability of results obtained on soft samples and living cells by a reliable method to calibrate AFM cantilevers.

Key words

Elasticity Stiffness Contact models Colloidal probes Calibration Deflection sensitivity Spring constant Force resolution 
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References

  1. 1.
    Block S (1990) Optical tweezers: a new tool for biophysics. In: Foskett JK, Grinstein S (eds) Noninvasive techniques in cell biology, Modern cell biology, vol 9. Wiley-Liss, New York, pp 375–402Google Scholar
  2. 2.
    Hochmuth RM (2000) Micropipette aspiration of living cells. J Biomech 33(1):15–22PubMedCrossRefGoogle Scholar
  3. 3.
    Laurent VM, Henon S, Planus E, Fodil R, Balland M, Isabey D, Gallet F (2002) Assessment of mechanical properties of adherent living cells by bead micromanipulation: comparison of magnetic twisting cytometry vs optical tweezers. J Biomech Eng 124(4):408–421PubMedCrossRefGoogle Scholar
  4. 4.
    Guck J, Ananthakrishnan R, Mahmood H, Moon TJ, Cunningham CC, Kas J (2001) The optical stretcher: a novel laser tool to micromanipulate cells. Biophys J 81(2):767–784.  https://doi.org/10.1016/S0006-3495(01)75740-2PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Rotsch C, Jacobson K, Radmacher M (1999) Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc Natl Acad Sci U S A 96(3):921–926PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Matzke R, Jacobson K, Radmacher M (2001) Direct, high-resolution measurement of furrow stiffening during division of adherent cells. Nat Cell Biol 3(6):607–610PubMedCrossRefGoogle Scholar
  7. 7.
    Laurent VM, Kasas S, Yersin A, Schaffer TE, Catsicas S, Dietler G, Verkhovsky AB, Meister JJ (2005) Gradient of rigidity in the lamellipodia of migrating cells revealed by atomic force microscopy. Biophys J 89(1):667–675.  https://doi.org/10.1529/biophysj.104.052316PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689.  https://doi.org/10.1016/j.cell.2006.06.044PubMedCrossRefGoogle Scholar
  9. 9.
    Vogel V, Sheetz M (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7(4):265–275.  https://doi.org/10.1038/nrm1890PubMedCrossRefGoogle Scholar
  10. 10.
    Lekka M, Laidler P, Gil D, Lekki J, Stachura Z, Hrynkiewicz AZ (1999) Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 28(4):312–316PubMedCrossRefGoogle Scholar
  11. 11.
    Prabhune M, Belge G, Dotzauer A, Bullerdiek J, Radmacher M (2012) Comparison of mechanical properties of normal and malignant thyroid cells. Micron 43(12):1267–1272.  https://doi.org/10.1016/j.micron.2012.03.023PubMedCrossRefGoogle Scholar
  12. 12.
    Gonzalez-Cruz RD, Fonseca VC, Darling EM (2012) Cellular mechanical properties reflect the differentiation potential of adipose-derived mesenchymal stem cells. Proc Natl Acad Sci U S A 109(24):E1523–E1529.  https://doi.org/10.1073/pnas.1120349109PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Wiesinger A, Peters W, Chappell D, Kentrup D, Reuter S, Pavenstadt H, Oberleithner H, Kumpers P (2013) Nanomechanics of the endothelial glycocalyx in experimental sepsis. PLoS One 8(11):e80905.  https://doi.org/10.1371/journal.pone.0080905PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Peters W, Kusche-Vihrog K, Oberleithner H, Schillers H (2015) Cystic fibrosis transmembrane conductance regulator is involved in polyphenol-induced swelling of the endothelial glycocalyx. Nanomedicine 11(6):1521–1530.  https://doi.org/10.1016/j.nano.2015.03.013PubMedCrossRefGoogle Scholar
  15. 15.
    Johnson KL (1985) Contact mechanics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  16. 16.
    Cohen SR, Kalfon-Cohen E (2013) Dynamic nanoindentation by instrumented nanoindentation and force microscopy: a comparative review. Beilstein J Nanotechnol 4:815–833.  https://doi.org/10.3762/bjnano.4.93PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Shi X, Zhao Y (2004) Comparison of various adhesion contact theories and the influence of dimensionless load parameter. J Adhesion Sci Technol 18(1):55–68CrossRefGoogle Scholar
  18. 18.
    Cappella B, Dietler G (1999) Force-Distance curves by atomic force microscopy. Surf Sci Rep 34:1–104CrossRefGoogle Scholar
  19. 19.
    Lin DC, Dimitriadis EK, Horkay F (2007) Robust strategies for automated AFM force curve analysis-II: adhesion-influenced indentation of soft, elastic materials. J Biomech Eng 129(6):904–912.  https://doi.org/10.1115/1.2800826PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Hertz H (1882) Ueber die Berührung fester elastischer Körper. Reine AngewMathematik 92:156–171Google Scholar
  21. 21.
    Sneddon IN (1965) The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 3(1):47–57CrossRefGoogle Scholar
  22. 22.
    Oliver WC, Pharr GM (1992) An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 7(6):1564–1583CrossRefGoogle Scholar
  23. 23.
    Johnson KL, Kendall K, Roberts AD (1971) Surface energy and the contact of elastic solids. Proc Roy Soc 324(1558):301–313CrossRefGoogle Scholar
  24. 24.
    Derjaguin BV, Muller VM, Toporov YP (1975) Effect of contact deformations on the adhesion of particles. J Colloid Interface Sci 53(2):314–326CrossRefGoogle Scholar
  25. 25.
    Tabor D (1977) Surface forces and surface interactions. J Colloid Interface Sci 58(1):2–13CrossRefGoogle Scholar
  26. 26.
    Ebenstein DM, Wahl KJ (2006) A comparison of JKR-based methods to analyze quasi-static and dynamic indentation force curves. J Colloid Interface Sci 298(2):652–662.  https://doi.org/10.1016/j.jcis.2005.12.062PubMedCrossRefGoogle Scholar
  27. 27.
    Maugis D (1992) Adhesion of spheres: The JKR-DMT transition using a dugale model. J Colloid Interface Sci 150(1):243–269CrossRefGoogle Scholar
  28. 28.
    Dugdale DS (1960) Yielding of steel sheets containing slits. J Mech Phys Solids 8(2):100–104CrossRefGoogle Scholar
  29. 29.
    Carpick RW, Ogletree DF, Salmeron M (1999) A general equation for fitting contact area and friction vs load measurements. J Colloid Interface Sci 211(2):395–400.  https://doi.org/10.1006/jcis.1998.6027PubMedCrossRefGoogle Scholar
  30. 30.
    Pietrement O, Troyon M (2000) General equations describing elastic indentation depth and normal contact stiffness versus load. J Colloid Interface Sci 226(1):166–171.  https://doi.org/10.1006/jcis.2000.6808PubMedCrossRefGoogle Scholar
  31. 31.
    Sokolov I, Iyer S, Subba-Rao V, Gaikwad RM, Woodworth CD (2007) Detection of surface brush on biological cells in vitro with atomic force microscopy. Appl Phys Lett 91:023901–023903CrossRefGoogle Scholar
  32. 32.
    Goicochea AG, Guardado SJ (2015) Computer simulations of the mechanical response of brushes on the surface of cancerous epithelial cells. Sci Rep 5:13218.  https://doi.org/10.1038/srep13218PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Dokukin M, Ablaeva Y, Kalaparthi V, Seluanov A, Gorbunova V, Sokolov I (2016) Pericellular brush and mechanics of guinea pig fibroblast cells studied with AFM. Biophys J 111(1):236–246.  https://doi.org/10.1016/j.bpj.2016.06.005PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Guz N, Dokukin M, Kalaparthi V, Sokolov I (2014) If cell mechanics can be described by elastic modulus: study of different models and probes used in indentation experiments. Biophys J 107(3):564–575.  https://doi.org/10.1016/j.bpj.2014.06.033PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Dokukin ME, Sokolov I (2012) On the measurement of rigidity modulus of soft material in nanoindentation experiments at small depth. Macromolecules 45(10):4277–4288CrossRefGoogle Scholar
  36. 36.
    Gavara N, Chadwick RS (2012) Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips. Nat Nanotechnol 7(11):733–736.  https://doi.org/10.1038/nnano.2012.163PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Cross SE, Jin YS, Rao J, Gimzewski JK (2009) Applicability of AFM in cancer detection. Nat Nanotechnol 4(2):72–73CrossRefGoogle Scholar
  38. 38.
    Tranchida D, Piccarolo S (2005) On the use of the nanoindentation unloading curve to measure the Young’s modulus of polymers on a nanometer scale. Macromol Rapid Commun 26(22):1800–1804CrossRefGoogle Scholar
  39. 39.
    Dimitriadis EK, Horkay F, Maresca J, Kachar B, Chadwick RS (2002) Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys J 82(5):2798–2810.  https://doi.org/10.1016/S0006-3495(02)75620-8PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Hassan E, Heinz WF, Antonik MD, D’Costa NP, Nageswaran S, Schoenenberger CA, Hoh JH (1998) Relative microelastic mapping of living cells by atomic force microscopy. Biophys J 74(3):1564–1578CrossRefGoogle Scholar
  41. 41.
    Zhao M, Srinivasan C, Burgess DJ, Huey BD (2006) Rate- and depth-dependent nanomechanical behavior of individual living Chinese hamster ovary cells probed by atomic force microscopy. J Mater Res 21(8):1906–1912CrossRefGoogle Scholar
  42. 42.
    Lieber SC, Aubry N, Pain J, Diaz G, Kim SJ, Vatner SF (2004) Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am J Physiol Heart Circ Physiol 287(2):H645–H651PubMedCrossRefGoogle Scholar
  43. 43.
    Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J Biomech 34(12):1545–1553PubMedCrossRefGoogle Scholar
  44. 44.
    Collinsworth AM, Zhang S, Kraus WE, Truskey GA (2002) Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Phys Cell Physiol 283(4):C1219–C1227CrossRefGoogle Scholar
  45. 45.
    Janovjak H, Struckmeier J, Muller DJ (2005) Hydrodynamic effects in fast AFM single-molecule force measurements. Eur Biophys J 34(1):91–96PubMedCrossRefGoogle Scholar
  46. 46.
    Horcas I, Fernandez R, Gomez-Rodriguez JM, Colchero J, Gomez-Herrero J, Baro AM (2007) WSXM: a software for scanning probe microscopy and a tool for nanotechnology. Rev Sci Instrum 78(1):013705.  https://doi.org/10.1063/1.2432410PubMedCrossRefGoogle Scholar
  47. 47.
    Hermanowicz P, Sarna M, Burda K, Gabrys H (2014) AtomicJ: an open source software for analysis of force curves. Rev Sci Instrum 85(6):063703.  https://doi.org/10.1063/1.4881683PubMedCrossRefGoogle Scholar
  48. 48.
    Necas D, Klapetek P (2013) One-dimensional autocorrelation and power spectrum density functions of irregular regions. Ultramicroscopy 124:13–19.  https://doi.org/10.1016/j.ultramic.2012.08.002PubMedCrossRefGoogle Scholar
  49. 49.
    Roduit C, Saha B, Alonso-Sarduy L, Volterra A, Dietler G, Kasas S (2012) OpenFovea: open-source AFM data processing software. Nat Methods 9(8):774–775.  https://doi.org/10.1038/nmeth.2112PubMedCrossRefGoogle Scholar
  50. 50.
    Carl P, Schillers H (2008) Elasticity measurement of living cells with atomic force microscopy: data aquisition and processing. Pflugers Arch 457(2):551–559PubMedCrossRefGoogle Scholar
  51. 51.
    Crick SL, Yin FC (2007) Assessing micromechanical properties of cells with atomic force microscopy: importance of the contact point. Biomech Model Mechanobiol 6(3):199–210.  https://doi.org/10.1007/s10237-006-0046-xPubMedCrossRefGoogle Scholar
  52. 52.
    Schillers H, Rianna C, Schape J, Luque T, Doschke H, Walte M, Uriarte JJ, Campillo N, Michanetzis GPA, Bobrowska J, Dumitru A, Herruzo ET, Bovio S, Parot P, Galluzzi M, Podesta A, Puricelli L, Scheuring S, Missirlis Y, Garcia R, Odorico M, Teulon JM, Lafont F, Lekka M, Rico F, Rigato A, Pellequer JL, Oberleithner H, Navajas D, Radmacher M (2017) Standardized nanomechanical atomic force microscopy procedure (SNAP) for measuring soft and biological samples. Sci Rep 7(1):5117.  https://doi.org/10.1038/s41598-017-05383-0PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Kasas S, Wang X, Hirling H, Marsault R, Huni B, Yersin A, Regazzi R, Grenningloh G, Riederer B, Forro L, Dietler G, Catsicas S (2005) Superficial and deep changes of cellular mechanical properties following cytoskeleton disassembly. Cell Motil Cytoskeleton 62(2):124–132.  https://doi.org/10.1002/cm.20086PubMedCrossRefGoogle Scholar
  54. 54.
    Costa KD, Yin FC (1999) Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy. J Biomech Eng 121(5):462–471PubMedCrossRefGoogle Scholar
  55. 55.
    Roduit C, Sekatski S, Dietler G, Catsicas S, Lafont F, Kasas S (2009) Stiffness tomography by atomic force microscopy. Biophys J 97(2):674–677.  https://doi.org/10.1016/j.bpj.2009.05.010PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    JPK_Instruments_AG Application note: determining the elastic modulus of biological samples using atomic force microscopy. https://www.jpk.com/app-technotes/applications_notes-cell-mechanics-and-adhesion
  57. 57.
    Girard PR, Nerem RM (1993) Endothelial cell signaling and cytoskeletal changes in response to shear stress. Front Med Biol Eng 5(1):31–36PubMedGoogle Scholar
  58. 58.
    Ko KS, McCulloch CA (2000) Partners in protection: interdependence of cytoskeleton and plasma membrane in adaptations to applied forces. J Membr Biol 174(2):85–95PubMedCrossRefGoogle Scholar
  59. 59.
    Targosz-Korecka M, Malek-Zietek KE, Brzezinka GD, Jaglarz M (2016) Morphological and nanomechanical changes in mechanosensitive endothelial cells induced by colloidal AFM probes. Scanning 38(6):654–664.  https://doi.org/10.1002/sca.21313PubMedCrossRefGoogle Scholar
  60. 60.
    Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463(7280):485–492.  https://doi.org/10.1038/nature08908PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    MacKintosh FC, Kas J, Janmey PA (1995) Elasticity of semiflexible biopolymer networks. Phys Rev Lett 75(24):4425–4428PubMedCrossRefGoogle Scholar
  62. 62.
    Gardel ML, Shin JH, MacKintosh FC, Mahadevan L, Matsudaira P, Weitz DA (2004) Elastic behavior of cross-linked and bundled actin networks. Science 304(5675):1301–1305.  https://doi.org/10.1126/science.1095087PubMedCrossRefGoogle Scholar
  63. 63.
    Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA (2005) Nonlinear elasticity in biological gels. Nature 435(7039):191–194.  https://doi.org/10.1038/nature03521PubMedCrossRefGoogle Scholar
  64. 64.
    Chaudhuri O, Parekh SH, Fletcher DA (2007) Reversible stress softening of actin networks. Nature 445(7125):295–298.  https://doi.org/10.1038/nature05459PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Wagner B, Tharmann R, Haase I, Fischer M, Bausch AR (2006) Cytoskeletal polymer networks: the molecular structure of cross-linkers determines macroscopic properties. Proc Natl Acad Sci U S A 103(38):13974–13978.  https://doi.org/10.1073/pnas.0510190103PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Jalilian I, Heu C, Cheng H, Freittag H, Desouza M, Stehn JR, Bryce NS, Whan RM, Hardeman EC, Fath T, Schevzov G, Gunning PW (2015) Cell elasticity is regulated by the tropomyosin isoform composition of the actin cytoskeleton. PLoS One 10(5):e0126214.  https://doi.org/10.1371/journal.pone.0126214PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Sweeney HL, Houdusse A (2010) Myosin VI rewrites the rules for myosin motors. Cell 141(4):573–582.  https://doi.org/10.1016/j.cell.2010.04.028PubMedCrossRefGoogle Scholar
  68. 68.
    Woolner S, Bement WM (2009) Unconventional myosins acting unconventionally. Trends Cell Biol 19(6):245–252.  https://doi.org/10.1016/j.tcb.2009.03.003PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Sellers JR (2000) Myosins: a diverse superfamily. Biochim Biophys Acta 1496(1):3–22PubMedCrossRefGoogle Scholar
  70. 70.
    Martens JC, Radmacher M (2008) Softening of the actin cytoskeleton by inhibition of myosin II. Pflugers Arch 456(1):95–100PubMedCrossRefGoogle Scholar
  71. 71.
    Koenderink GH, Dogic Z, Nakamura F, Bendix PM, MacKintosh FC, Hartwig JH, Stossel TP, Weitz DA (2009) An active biopolymer network controlled by molecular motors. Proc Natl Acad Sci U S A 106(36):15192–15197.  https://doi.org/10.1073/pnas.0903974106PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Watanabe T, Hosoya H, Yonemura S (2007) Regulation of myosin II dynamics by phosphorylation and dephosphorylation of its light chain in epithelial cells. Mol Biol Cell 18(2):605–616.  https://doi.org/10.1091/mbc.E06-07-0590PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104(Pt 3):613–627PubMedGoogle Scholar
  74. 74.
    Placais PY, Balland M, Guerin T, Joanny JF, Martin P (2009) Spontaneous oscillations of a minimal actomyosin system under elastic loading. Phys Rev Lett 103(15):158102PubMedCrossRefGoogle Scholar
  75. 75.
    Hong Z, Sun Z, Li M, Li Z, Bunyak F, Ersoy I, Trzeciakowski JP, Staiculescu MC, Jin M, Martinez-Lemus L, Hill MA, Palaniappan K, Meininger GA (2014) Vasoactive agonists exert dynamic and coordinated effects on vascular smooth muscle cell elasticity, cytoskeletal remodelling and adhesion. J Physiol 592(6):1249–1266.  https://doi.org/10.1113/jphysiol.2013.264929PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Na S, Trache A, Trzeciakowski J, Sun Z, Meininger GA, Humphrey JD (2008) Time-dependent changes in smooth muscle cell stiffness and focal adhesion area in response to cyclic equibiaxial stretch. Ann Biomed Eng 36(3):369–380.  https://doi.org/10.1007/s10439-008-9438-7PubMedCrossRefGoogle Scholar
  77. 77.
    Zhu Y, Qiu H, Trzeciakowski JP, Sun Z, Li Z, Hong Z, Hill MA, Hunter WC, Vatner DE, Vatner SF, Meininger GA (2012) Temporal analysis of vascular smooth muscle cell elasticity and adhesion reveals oscillation waveforms that differ with aging. Aging Cell 11(5):741–750.  https://doi.org/10.1111/j.1474-9726.2012.00840.xPubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Schillers H, Walte M, Urbanova K, Oberleithner H (2010) Real-time monitoring of cell elasticity reveals oscillating myosin activity. Biophys J 99(11):3639–3646.  https://doi.org/10.1016/j.bpj.2010.09.048PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Ishiwata S, Shimamoto Y, Suzuki M, Sasaki D (2007) Regulation of muscle contraction by Ca2+ and ADP: focusing on the auto-oscillation (SPOC). Adv Exp Med Biol 592:341–358PubMedCrossRefGoogle Scholar
  80. 80.
    Shimamoto Y, Suzuki M, Ishiwata S (2008) Length-dependent activation and auto-oscillation in skeletal myofibrils at partial activation by Ca2+. Biochem Biophys Res Commun 366(1):233–238.  https://doi.org/10.1016/j.bbrc.2007.11.123PubMedCrossRefGoogle Scholar
  81. 81.
    Vegh AG, Fazakas C, Nagy K, Wilhelm I, Krizbai IA, Nagyoszi P, Szegletes Z, Varo G (2011) Spatial and temporal dependence of the cerebral endothelial cells elasticity. J Mol Recognit 24(3):422–428.  https://doi.org/10.1002/jmr.1107PubMedCrossRefGoogle Scholar
  82. 82.
    Martin AC (2010) Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol 341(1):114–125.  https://doi.org/10.1016/j.ydbio.2009.10.031PubMedCrossRefGoogle Scholar
  83. 83.
    Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457(7228):495–499.  https://doi.org/10.1038/nature07522PubMedCrossRefGoogle Scholar
  84. 84.
    Munro E, Nance J, Priess JR (2004) Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev Cell 7(3):413–424.  https://doi.org/10.1016/j.devcel.2004.08.001PubMedCrossRefGoogle Scholar
  85. 85.
    Paluch E, Piel M, Prost J, Bornens M, Sykes C (2005) Cortical actomyosin breakage triggers shape oscillations in cells and cell fragments. Biophys J 89(1):724–733.  https://doi.org/10.1529/biophysj.105.060590PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Pecreaux J, Roper JC, Kruse K, Julicher F, Hyman AA, Grill SW, Howard J (2006) Spindle oscillations during asymmetric cell division require a threshold number of active cortical force generators. Curr Biol 16(21):2111–2122.  https://doi.org/10.1016/j.cub.2006.09.030PubMedCrossRefGoogle Scholar
  87. 87.
    Martin P, Bozovic D, Choe Y, Hudspeth AJ (2003) Spontaneous oscillation by hair bundles of the bullfrog’s sacculus. J Neurosci 23(11):4533–4548PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Schillers H (2014) Restless cell syndrome. J Physiol 592(Pt 6):1175–1176.  https://doi.org/10.1113/jphysiol.2014.271759PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kruse K, Julicher F (2005) Oscillations in cell biology. Curr Opin Cell Biol 17(1):20–26.  https://doi.org/10.1016/j.ceb.2004.12.007PubMedCrossRefGoogle Scholar
  90. 90.
    Charras GT, Horton MA (2002) Determination of cellular strains by combined atomic force microscopy and finite element modeling. Biophys J 83(2):858–879.  https://doi.org/10.1016/S0006-3495(02)75214-4PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Radmacher M, Fritz M, Kacher CM, Cleveland JP, Hansma PK (1996) Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J 70(1):556–567PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Rigato A, Rico F, Eghiaian F, Piel M, Scheuring S (2015) Atomic force microscopy mechanical mapping of micropatterned cells shows adhesion geometry-dependent mechanical response on local and global scales. ACS Nano 9(6):5846–5856.  https://doi.org/10.1021/acsnano.5b00430PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Puricelli L, Galluzzi M, Schulte C, Podesta A, Milani P (2015) Nanomechanical and topographical imaging of living cells by atomic force microscopy with colloidal probes. Rev Sci Instrum 86(3):033705.  https://doi.org/10.1063/1.4915896PubMedCrossRefGoogle Scholar
  94. 94.
    Domke J, Radmacher M (1998) Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir 14:3320–3325CrossRefGoogle Scholar
  95. 95.
    Labuda A (2012) Adventures in atomic force microscopy towards the study of the solid-liquid interface. McGill University, Montreal http://digitool.Library.McGill.CA:80/R/-?func=dbin-jump-full&object_id=110355&silo_library=GEN01
  96. 96.
    Labuda A, Kocun M, Lysy M, Walsh T, Meinhold J, Proksch T, Meinhold W, Anderson C, Proksch R (2016) Calibration of higher eigenmodes of cantilevers. Rev Sci Instrum 87(7):073705.  https://doi.org/10.1063/1.4955122PubMedCrossRefGoogle Scholar
  97. 97.
    Habibnejad Korayem M, Jiryaei Sharahi H, Habibnejad Korayem A (2012) Comparison of frequency response of atomic force microscopy cantilevers under tip-sample interaction in air and liquids. Scient Iran 19(1):106–112.  https://doi.org/10.1016/j.scient.2011.12.009CrossRefGoogle Scholar
  98. 98.
    Lubbe J, Temmen M, Rode S, Rahe P, Kuhnle A, Reichling M (2013) Thermal noise limit for ultra-high vacuum noncontact atomic force microscopy. Beilstein J Nanotechnol 4:32–44.  https://doi.org/10.3762/bjnano.4.4PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Gates RS, Osborn WA, Pratt JR (2013) Experimental determination of mode correction factors for thermal method spring constant calibration of AFM cantilevers using laser Doppler vibrometry. Nanotechnology 24(25):255706.  https://doi.org/10.1088/0957-4484/24/25/255706PubMedCrossRefGoogle Scholar
  100. 100.
    Alexander S, Hellemans L, Marti O, Schneir J, Elings V, Hansma PK, Longmire M, Gurley J (1989) An atomic-resolution atomic-force microscope implemented using an optical lever. J Appl Phys 65(1):164–167CrossRefGoogle Scholar
  101. 101.
    te Riet J, Katan AJ, Rankl C, Stahl SW, van Buul AM, Phang IY, Gomez-Casado A, Schon P, Gerritsen JW, Cambi A, Rowan AE, Vancso GJ, Jonkheijm P, Huskens J, Oosterkamp TH, Gaub H, Hinterdorfer P, Figdor CG, Speller S (2011) Interlaboratory round robin on cantilever calibration for AFM force spectroscopy. Ultramicroscopy 111(12):1659–1669.  https://doi.org/10.1016/j.ultramic.2011.09.012PubMedCrossRefGoogle Scholar
  102. 102.
    Burnham NA, Chen X, Hodges CS, Matai GA, Thoreson EJ, Roberts CJ, Davies MC, Tendler SBJ (2003) Comparison of calibration methods for atomic-force microscopy cantilevers. Nanotechnology 14(1):1–6CrossRefGoogle Scholar
  103. 103.
    Gates RS, Reitsma MG, Kramar JA, Pratt JR (2011) Atomic force microscope cantilever flexural stiffness calibration: toward a standard traceable method. J Res Natl Inst Stand Technol 116(4):703–727PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Butt H-J, Jaschke M (1995) Calculation of thermal noise in atomic force microscopy. Nanotechnology 6:1–7CrossRefGoogle Scholar
  105. 105.
    Hutter JL, Bechhoefer J (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64(7):1868–1873CrossRefGoogle Scholar
  106. 106.
    Cleveland JP, Manne S, Bocek D, Hansma PK (1993) A nondestructive method for determining the spring constant of cantilevers for scanning force microscopy. Rev Sci Instrum 64(2):403–405CrossRefGoogle Scholar
  107. 107.
    Sader JE (2002) Calibration of atomic force microscope cantilevers. In: Hubbard A (ed) Encyclopedia of surface and colloid science. Marcel Dekker Inc., New York, pp 846–856Google Scholar
  108. 108.
    Walters DA, Cleveland JP, Thomson NH, Hansma PK, Wendman MA, Gurley G, Elings V (1996) Short cantilevers for atomic force microscopy. Rev Sci Instrum 67(10):3583–3590.  https://doi.org/10.1063/1.1147177CrossRefGoogle Scholar
  109. 109.
    Pirzer T, Hugel T (2009) Atomic force microscopy spring constant determination in viscous liquids. Rev Sci Instrum 80(3):035110.  https://doi.org/10.1063/1.3100258PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Hutter JL (2005) Comment on tilt of atomic force microscope cantilevers: effect on spring constant and adhesion measurements. Langmuir 21(6):2630–2632.  https://doi.org/10.1021/la047670tPubMedCrossRefGoogle Scholar
  111. 111.
    Ohler B (2007) Application note: practical advice on the determination of cantilever spring constants. http://nanoscaleworld.bruker-axs.com/nanoscaleworld/media/p/143.aspx. Veeco Instruments
  112. 112.
    Ohler B (2007) Cantilever spring constant calibration using laser Doppler vibrometry. Rev Sci Instrum 78(6):063701.  https://doi.org/10.1063/1.2743272PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Physiology IIUniversity of MünsterMünsterGermany

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