If Cell Mechanics Can Be Described by Elastic Modulus: Study of Different Models and Probes Used in Indentation Experiments

Biophysical Journal

Volumn 107, Issue 3, 2014, Pages 564-575

  Guz, Nataliia ^a   Dokukin, Maxim ^b   Kalaparthi, Vivekanand ^b   Sokolov, Igor ^b,c  

^a CLARKSON UNIVERSITY   (United States)

^b Tufts University   (United States)

^c TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MODEL; CELL CULTURE; CELL SURFACE; EPITHELIUM CELL; GLYCOCALYX; HUMAN; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE; YOUNG MODULUS;

CELL SURFACE EXTENSIONS; CELLS, CULTURED; ELASTIC MODULUS; EPITHELIAL CELLS; GLYCOCALYX; HUMANS; MODELS, BIOLOGICAL;

EID: 84905643384     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.06.033     Document Type: Article

References (57)

1. C.G. Galbraith, and M.P. Sheetz Forces on adhesive contacts affect cell function Curr. Opin. Cell Biol. 10 1998 566 571
2. V. Vogel, and M. Sheetz Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 7 2006 265 275
3. O. Chaudhuri, and D.J. Mooney Stem-cell differentiation: anchoring cell-fate cues Nat. Mater. 11 2012 568 569
4. P. Ulrich, and X. Zhang Pharmacological reversal of advanced glycation end-product-mediated protein crosslinking Diabetologia 40 Suppl 2 1997 S157 S159
5. R.J. Castellani, and P.L. Harris M.A. Smith Active glycation in neurofibrillary pathology of Alzheimer disease: Nε-(carboxymethyl) lysine and hexitol-lysine Free Radic. Biol. Med. 31 2001 175 180
6. R. Bucala, and A. Cerami Advanced glycosylation: chemistry, biology, and implications for diabetes and aging Adv. Pharmacol. 23 1992 1 34
7. G.P. Dimri, and X. Lee J. Campisi A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proc. Natl. Acad. Sci. USA 92 1995 9363 9367
8. S. Suresh Biomechanics and biophysics of cancer cells Acta Biomater. 3 2007 413 438
9. S.E. Cross, and Y.S. Jin J.K. Gimzewski Nanomechanical analysis of cells from cancer patients Nat. Nanotechnol. 2 2007 780 783
10. I. Sokolov, S. Iyer, and C.D. Woodworth Recover of elasticity of aged human epithelial cells in-vitro Nanomed. Nanotechnol., Biol. Med. 2 2006 31 36
11. G.B. Nash, and E. O'Brien J.A. Dormandy Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum Blood 74 1989 855 861
12. J. Li, and M. Dao S. Suresh Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte Biophys. J. 88 2005 3707 3719
13. M.J. Paszek, and N. Zahir V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254
14. M. Lekka, and P. Laidler Applicability of AFM in cancer detection Nat. Nanotechnol. 4 2009 72 73
15. S. Iyer, and R.M. Gaikwad I. Sokolov AFM detects differences in the surface brush on normal and cancerous cervical cells Nat. Nanotechnol. 4 2009 389 393
16. L. Bastatas, and D. Martinez-Marin S. Park AFM nano-mechanics and calcium dynamics of prostate cancer cells with distinct metastatic potential Biochim. Biophys. Acta 1820 2012 1111 1120
17. Q.S. Li, and G.Y. Lee C.T. Lim AFM indentation study of breast cancer cells Biochem. Biophys. Res. Commun. 374 2008 609 613
18. Z.L. Zhou, and A.H. Ngan A.X. Wang Reliable measurement of elastic modulus of cells by nanoindentation in an atomic force microscope J. Mech. Behav. Biomed. Mater. 8 2012 134 142
19. L.D. Landau, and E.M. Lifshits L.P. Pitaevskii Theory of Elasticity 1986 Pergamon Press New York
20. R.T. Adkins Information Sources in Polymers and Plastics 1989 Bowker-Saur London, UK
21. S. Kalpakjian, and S.R. Schmid Manufacturing Processes for Engineering Materials 2008 Pearson Education Upper Saddle River, NJ
22. M.E. Dokukin, and I. Sokolov On the measurements of rigidity modulus of soft materials in nanoindentation experiments at small depth Macromolecules 45 2012 4277 4288
23. A.E. Pelling, and S. Sehati J.K. Gimzewski Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae Science 305 2004 1147 1150
24. I. Sokolov, M. Firtel, and G.S. Henderson In situ high-resolution AFM imaging of biological surfaces J. Vac. Sci. Technol. B 14 1996 674 678
25. T.K. Berdyyeva, C.D. Woodworth, and I. Sokolov Human epithelial cells increase their rigidity with aging in vitro: direct measurements Phys. Med. Biol. 50 2005 81 92
26. J.H. Hoh, and C.A. Schoenenberger Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy J. Cell Sci. 107 1994 1105 1114
27. G. Bischoff, and A. Bernstein H.J. Hein Imaging living chondrocyte surface structures with AFM contact mode Methods Mol. Biol. 242 2004 105 124
28. J.L. Alonso, and W.H. Goldmann Feeling the forces: atomic force microscopy in cell biology Life Sci. 72 2003 2553 2560
29. M. Lekka, and D. Gil P. Laidler Cancer cell detection in tissue sections using AFM Arch. Biochem. Biophys. 518 2012 151 156
30. I. Sokolov, and S. Iyer C.D. Woodworth Detection of surface brush on biological cells in vitro with atomic force microscopy Appl. Phys. Lett. 91 2007 023902
31. M.E. Dokukin, N.V. Guz, and I. Sokolov Quantitative study of the elastic modulus of loosely attached cells in AFM indentation experiments Biophys. J. 104 2013 2123 2131
32. R.M. Gaikwad, and M.E. Dokukin I. Sokolov Detection of cancerous cervical cells using physical adhesion of fluorescent silica particles and centripetal force Analyst (Lond.) 136 2011 1502 1506
33. C.D. Woodworth, J. Doniger, and J.A. DiPaolo Immortalization of human foreskin keratinocytes by various human papillomavirus DNAs corresponds to their association with cervical carcinoma J. Virol. 63 1989 159 164
34. D. Gaiotti, J. Chung, M. Iglesias, M. Nees, P.D. Baker, C.H. Evans, and C.D. Woodworth Tumor necrosis factor-alpha promotes human papillomavirus (HPV) E6/E7 RNA expression and cyclin-dependent kinase activity in HPV-immortalized keratinocytes by a ras-dependent pathway Mol. Carcinog. 27 2000 97 109
35. D.O. Volkov, and P.R.V. Dandu I. Sokolov Influence of adhesion of silica and ceria abrasive nanoparticles on chemical-mechanical planarization of silica surfaces Appl. Surf. Sci. 257 2011 8518 8524
36. S. Iyer, and C.D. Woodworth I. Sokolov Towards nonspecific detection of malignant cervical cells with fluorescent silica beads Small 5 2009 2277 2284
37. M.H. Zhao, and C. Srinivasan B.D. Huey Rate- and depth-dependent nanomechanical behavior of individual living Chinese hamster ovary cells probed by atomic force microscopy J. Mater. Res. 21 2006 1906 1912
38. I.N. Sneddon The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile Int. J. Eng. Sci. 3 1965 47 57
39. H.R. Hertz On contact between elastic bodies [Ueber die berührung fester elastischer körper] J. Reine Angew.Math. (Crelle's J.) 94 1882 156 171
40. I. Sokolov, and S. Iyer C.D. Woodworth Detection of surface brush on biological cells in vitro with atomic force microscopy Appl. Phys. Lett. 91 2007 023901
41. C. Rotsch, and F. Braet M. Radmacher AFM imaging and elasticity measurements on living rat liver macrophages Cell Biol. Int. 21 1997 685 696
42. H.W. Wu, T. Kuhn, and V.T. Moy Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking Scanning 20 1998 389 397
43. R. Matzke, K. Jacobson, and M. Radmacher Direct, high-resolution measurement of furrow stiffening during division of adherent cells Nat. Cell Biol. 3 2001 607 610
44. S.E. Cross, and Y.S. Jin J.K. Gimzewski AFM-based analysis of human metastatic cancer cells Nanotechnology 19 2008 384003
45. P. Carl, and H. Schillers Elasticity measurement of living cells with an atomic force microscope: data acquisition and processing Pflugers Arch. 457 2008 551 559
46. I. Sokolov, M.E. Dokukin, and N.V. Guz Method for quantitative measurements of the elastic modulus of biological cells in AFM indentation experiments Methods 60 2013 202 213
47. X. Wang, and A.A. Shah K.T. Wan Glycoprotein mucin molecular brush on cancer cell surface acting as mechanical barrier against drug delivery Appl. Phys. Lett. 97 2010 263703
48. J. Israelachivili Intermolecular and Surface Forces 2011 Academic Press Burlington, MA
49. H.J. Butt, B. Cappella, and M. Kappl Force measurements with the atomic force microscope: technique, interpretation and applications Surf. Sci. Rep. 59 2005 1 152
50. H.J. Butt, and M. Kappl J. Rühe Steric forces measured with the atomic force microscope at various temperatures Langmuir 15 1999 2559 2565
51. I.Y. Sokolov On the limits on spectroscopic ability of AFM and interaction between an AFM tip and a sample Surf. Sci. 311 1994 287 294
52. I. Sokolov, and V. Kalaparthi M.E. Dokukin On averaging force curves over heterogeneous surfaces in atomic force microscopy Ultramicroscopy 121 2012 16 24
53. M.E. Dokukin, and I. Sokolov Quantitative mapping of the elastic modulus of soft materials with HarmoniX and PeakForce QNM AFM modes Langmuir 28 2012 16060 16071
54. E.K. Dimitriadis, and F. Horkay R.S. Chadwick Determination of elastic moduli of thin layers of soft material using the atomic force microscope Biophys. J. 82 2002 2798 2810
55. K.D. Costa, and F.C.P. Yin Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy J. Biomech. Eng. 121 1999 462 471
56. R. Vargas-Pinto, and H. Gong M. Johnson The effect of the endothelial cell cortex on atomic force microscopy measurements Biophys. J. 105 2013 300 309
57. A. Fuhrmann, and J.R. Staunton R. Ros AFM stiffness nanotomography of normal, metaplastic and dysplastic human esophageal cells Phys. Biol. 8 2011 015007