Local viscoelastic properties of live cells investigated using dynamic and quasi-static atomic force microscopy methods

Biophysical Journal

Volumn 106, Issue 5, 2014, Pages 1033-1043

  Cartagena, Alexander ^a   Raman, Arvind ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL LINE; CYTOLOGY; ELASTICITY; FIBROBLAST; METHODOLOGY; RAT; VISCOSITY;

ANIMALS; CELL LINE; ELASTICITY; FIBROBLASTS; MICROSCOPY, ATOMIC FORCE; RATS; VISCOSITY;

EID: 84901740791     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.12.037     Document Type: Article

References (73)

1. S. Suresh Biomechanics and biophysics of cancer cells Acta Biomater. 3 2007 413 438
2. J. Guck, and F. Lautenschläger M. Beil Critical review: cellular mechanobiology and amoeboid migration Integr. Biol. (Camb) 2 2010 575 583
3. E.U. Azeloglu, and K.D. Costa Atomic force microscopy in mechanobiology: measuring microelastic heterogeneity of living cells Methods Mol. Biol. 736 2011 303 329
4. A. Raman, and S. Trigueros S.A. Contera Mapping nanomechanical properties of live cells using multi-harmonic atomic force microscopy Nat. Nanotechnol. 6 2011 809 814
5. C.A.J. Putman, and K.O. van der Werf J. Greve Viscoelasticity of living cells allows high resolution imaging by tapping mode atomic force microscopy Biophys. J. 67 1994 1749 1753
6. A.R. Bausch, W. Möller, and E. Sackmann Measurement of local viscoelasticity and forces in living cells by magnetic tweezers Biophys. J. 76 1999 573 579
7. B. Fabry, and G.N. Maksym J.J. Fredberg Scaling the microrheology of living cells Phys. Rev. Lett. 87 2001 148102
8. X. Trepat, and L. Deng J.J. Fredberg Universal physical responses to stretch in the living cell Nature 447 2007 592 595
9. V. Vadillo-Rodriguez, and J.R. Dutcher Dynamic viscoelastic behavior of individual Gram-negative bacterial cells Soft Matter 5 2009 5012 5019
10. D.E. Ingber The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering? Cell 75 1993 1249 1252
11. D.J. Montell Morphogenetic cell movements: diversity from modular mechanical properties Science 322 2008 1502 1505
12. N. Wang, J.P. Butler, and D.E. Ingber Mechanotransduction across the cell surface and through the cytoskeleton Science 260 1993 1124 1127
13. D.E. Ingber Tensegrity: the architectural basis of cellular mechanotransduction Annu. Rev. Physiol. 59 1997 575 599
14. D.E. Ingber Tensegrity I. Cell structure and hierarchical systems biology J. Cell Sci. 116 2003 1157 1173
15. C. Rotsch, K. Jacobson, and M. Radmacher Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy Proc. Natl. Acad. Sci. USA 96 1999 921 926
16. D. Yamazaki, S. Kurisu, and T. Takenawa Regulation of cancer cell motility through actin reorganization Cancer Sci. 96 2005 379 386
17. D.E. Discher, P. Janmey, and Y.L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143
18. C.M. Lo, and H.B. Wang Y.L. Wang Cell movement is guided by the rigidity of the substrate Biophys. J. 79 2000 144 152
19. J. Guck, and S. Schinkinger C. Bilby Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence Biophys. J. 88 2005 3689 3698
20. S.E. Cross, and Y.S. Jin J.K. Gimzewski Nanomechanical analysis of cells from cancer patients Nat. Nanotechnol. 2 2007 780 783
21. E.M. Darling, and S. Zauscher F. Guilak A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? Biophys. J. 92 2007 1784 1791
22. S.E. Cross, and Y.S. Jin J.K. Gimzewski AFM-based analysis of human metastatic cancer cells Nanotechnology 19 2008 384003
23. E.C. Faria, and N. Ma R.D. Snook Measurements of elastic properties of prostate cancer cells using AFM Analyst (Lond.) 133 2008 1498 1500
24. S. Kumar, and V.M. Weaver Mechanics, malignancy, and metastasis: the force journey of a tumor cell Cancer Metastasis Rev. 28 2009 113 127
25. J.G. Goetz, and S. Minguet M.A. Del Pozo Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis Cell 146 2011 148 163
26. A.E. Pelling, and F.S. Veraitch M.A. Horton Mechanical dynamics of single cells during early apoptosis Cell Motil. Cytoskeleton 66 2009 409 422
27. C.W. Gourlay, and K.R. Ayscough The actin cytoskeleton: a key regulator of apoptosis and aging? Nat. Rev. Mol. Cell Biol. 6 2005 583 589
28. D. Ilić, and Y. Furuta T. Yamamoto Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice Nature 377 1995 539 544
29. R.J. Pelham Jr.; and Y. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. USA 94 1997 13661 13665
30. N.Q. Balaban, and U.S. Schwarz B. Geiger Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates Nat. Cell Biol. 3 2001 466 472
31. D. Riveline, and E. Zamir A.D. Bershadsky Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism J. Cell Biol. 153 2001 1175 1186
32. B.D. Matthews, and D.R. Overby D.E. Ingber Mechanical properties of individual focal adhesions probed with a magnetic microneedle Biochem. Biophys. Res. Commun. 313 2004 758 764
33. J.L. Maciaszek, and G. Lykotrafitis Sickle cell trait human erythrocytes are significantly stiffer than normal J. Biomech. 44 2011 657 661
34. C. Rotsch, and M. Radmacher Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study Biophys. J. 78 2000 520 535
35. K. Bhadriraju, and L.K. Hansen Extracellular matrix- and cytoskeleton-dependent changes in cell shape and stiffness Exp. Cell Res. 278 2002 92 100
36. R. Brandt Cytoskeletal mechanisms of neuronal degeneration Cell Tissue Res. 305 2001 255 265
37. K.J. van Vliet, G. Bao, and S. Suresh The biomechanics toolbox: experimental approaches for living cells and biomolecules Acta Biomater. 51 2003 5881 5905
38. G. Bao, and S. Suresh Cell and molecular mechanics of biological materials Nat. Mater. 2 2003 715 725
39. M. Benoit, and H.E. Gaub Measuring cell adhesion forces with the atomic force microscope at the molecular level Cells Tissues Organs (Print) 172 2002 174 189
40. M. Arnoldi, and M. Fritz A. Boulbitch Bacterial turgor pressure can be measured by atomic force microscopy Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 62 1 Pt B 2000 1034 1044
41. A. Touhami, B. Nysten, and Y.F. Dufrêne Nanoscale mapping of the elasticity of microbial cells by atomic force microcopy Langmuir 19 2003 4539 4543
42. V. Dupres, and F.D. Menozzi Y.F. Dufrêne Nanoscale mapping and functional analysis of individual adhesins on living bacteria Nat. Methods 2 2005 515 520
43. G. Longo, and L.M. Rio S. Kasas Force volume and stiffness tomography investigation on the dynamics of stiff material under bacterial membranes J. Mol. Recognit. 25 2012 278 284
44. Y.F. Dufrêne, and D. Martínez-Martín D.J. Müller Multiparametric imaging of biological systems by force-distance curve-based AFM Nat. Methods 10 2013 847 854
45. M. Radmacher, and M. Fritz P.K. Hansma Measuring the viscoelastic properties of human platelets with the atomic force microscope Biophys. J. 70 1996 556 567
46. E. A-Hassan, and W.F. Heinz J.H. Hoh Relative microelastic mapping of living cells by atomic force microscopy Biophys. J. 74 1998 1564 1578
47. H. Haga, and S. Sasaki T. Sambongi Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton Ultramicroscopy 82 2000 253 258
48. J. Solon, and I. Levental P.A. Janmey Fibroblast adaptation and stiffness matching to soft elastic substrates Biophys. J. 93 2007 4453 4461
49. E.M. Darling Force scanning: a rapid, high-resolution approach for spatial mechanical property mapping Nanotechnology 22 2011 175707
50. M. Prabhune, and G. Belge M. Radmacher Comparison of mechanical properties of normal and malignant thyroid cells Micron 43 2012 1267 1272
51. J. Alcaraz, and L. Buscemi D. Navajas Microrheology of human lung epithelial cells measured by atomic force microscopy Biophys. J. 84 2003 2071 2079
52. N. Gavara, and R.S. Chadwick Determination of the elastic moduli of thin samples and adherent cells using conical atomic force microscope tips Nat. Nanotechnol. 7 2012 733 736
53. E.M. Darling, S. Zauscher, and F. Guilak Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy Osteoarthritis Cartilage 14 2006 571 579
54. V. Vadillo-Rodriguez, T.J. Beveridge, and J.R. Dutcher Surface viscoelasticity of individual Gram-negative bacterial cells measured using atomic force microscopy J. Bacteriol. 190 2008 4225 4232
55. A.R. Bausch, and F. Ziemann E. Sackmann Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry Biophys. J. 75 1998 2038 2049
56. R.C. Tung, A. Jana, and A. Raman Hydrodynamic loading of microcantilevers oscillating near rigid walls J. Appl. Phys. 104 2008 114905
57. R.E. Mahaffy, and C.K. Shih J. Käs Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells Phys. Rev. Lett. 85 2000 880 883
58. R.E. Mahaffy, and S. Park C.K. Shih Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy Biophys. J. 86 2004 1777 1793
59. X. Xu, and A. Raman Comparative dynamics of magnetically, acoustically, and Brownian motion driven microcantilevers in liquids J. Appl. Phys. 102 2007 034303
60. X. Xu, M. Koslowski, and A. Raman Dynamics of surface-coupled microcantilevers in force modulation atomic force microscopy - magnetic vs. dither piezo excitation J. Appl. Phys. 111 2012 054303
61. D. Kiracofe, and A. Raman Quantitative force and dissipation measurements in liquids using piezo-excited atomic force microscopy: a unifying theory Nanotechnology 22 2011 485502
62. U. Rabe, K. Janser, and W. Arnold Vibrations of free and surface-coupled atomic force microscope cantilevers: theory and experiment Rev. Sci. Instrum. 67 1996 3281 3293
63. S. de Beer, D. van den Ende, and F. Mugele Atomic force microscopy cantilever dynamics in liquid in the presence of tip sample interaction Appl. Phys. Lett. 93 2008 253106
64. J.L. Hutter, and J. Bechhoefer Calibration of atomic-force microscope tips Rev. Sci. Instrum. 64 1993 1868 1873
65. H.-J. Butt, and M. Jaschke Calculation of thermal noise in atomic force microscopy Nanotechnology 6 1995 1 7
66. X. Xu, and C. Carrasco A. Raman Unmasking imaging forces on soft biological samples in liquids when using dynamic atomic force microscopy: a case study on viral capsids Biophys. J. 95 2008 2520 2528
67. I. Sokolov, and S. Lyer C.D. Woodworth Detection of surface brush on biological cells in vitro with atomic force microscopy Appl. Phys. Lett. 91 2007 023902
68. S. Iyer, and R.M. Gaikwad I. Sokolov Atomic force microscopy detects differences in the surface brush of normal and cancerous cells Nat. Nanotechnol. 4 2009 389 393
69. Y. Jamali, M. Azimi, and M.R.K. Mofrad A sub-cellular viscoelastic model for cell population mechanics PLoS ONE 5 2010 e12097
70. R. Proksch, and D.G. Yablon Loss tangent imaging: theory and simulations of repulsive-mode tapping mode atomic force microscopy Appl. Phys. Lett. 100 2012 073106
71. A. Cartagena, and M. Hernando-Pérez A. Raman Mapping in vitro local material properties of intact and disrupted virions at high resolution using multi-harmonic atomic force microscopy Nanoscale 5 2013 4729 4736
72. A. Dulebo, and J. Preiner P. Hinterdorfer Second harmonic atomic force microscopy imaging of live and fixed mammalian cells Ultramicroscopy 109 2009 1056 1060
73. Kiracofe, D.; J. Melcher,.; S. Hu. 2013. VEDA: virtual environment for dynamic AFM. https://nanohub.org/resources/veda. http://dx.doi.org/10.4231/ D3KW57J1T.