A Three-Dimensional Viscoelastic Model for Cell Deformation with Experimental Verification

Biophysical Journal

Volumn 85, Issue 5, 2003, Pages 3336-3349

  Karcher, Hélène ^a   Lammerding, Jan ^b   Huang, Hayden ^b   Lee, Richard T ^b   Kamm, Roger D ^a,c   Kaazempur Mofrad, Mohammad R ^a  

^a Massachusetts Institute of Technology   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN 3T3; CELL STRUCTURE; CYTOMETRY; CYTOSKELETON; FIBROBLAST; FINITE ELEMENT ANALYSIS; MAGNETOCYTOMETRY; MODEL; MONOLAYER CULTURE; MOUSE; NONHUMAN; STRESS STRAIN RELATIONSHIP; VISCOELASTICITY;

ANIMALIA;

EID: 0242322436     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74753-5     Document Type: Article

References (44)

1. Bathe, K. J. 1996. Finite Element Procedures. Prentice Hall, Englewood Cliffs, NJ.
2. Balaban, N. Q., U. S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, I. Sabanay, D. Mahalu, S. Safran, A. Bershadsky, L. Addadi, and B. Geiger. 2001. Force and focal adhesion assembly: a close relationship studied using elastic micropattemed substrates. Nat. Cell Biol. 3:466-472.
3. Bausch, A. R., U. Hellerer, M. Essler, M. Aepfelbacher, and E. Sackmann. 2001. Rapid stiffening of integrin receptor-actin linkages in endothelial cells stimulated with thrombin: a magnetic bead microrheology study. Biophys. J. 80:2649-2657.
4. Bausch, A. R., F. Ziemann, A. A. Boulbitch, K. Jacobson, and E. Sackmann. 1998. Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophys. J. 75:2038-2049.
5. Boulbitch, A. A. 1999. Strain of a biomembrane caused by local tangential force: application to magnetic tweezer measurements. Phys. Rev. E. 59: 3402-3407.
6. Brown, T. D. 2000. Techniques for mechanical stimulation of cells in vitro: a review. J. Biomech. 33:3-14.
7. Charras, G. T., and M. A. Horton. 2002a. Determination of cellular strains by combined atomic force microscopy and finite element modeling. Biophys. J. 83:858-879.
8. Charras, G. T., and M. A. Horton. 2002b. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys. J. 82:2970-2981.
9. Charras, G. T., P. P. Lehenkari, and M. A. Horton. 2001. Atomic force microscopy can be used to mechanically stimulate osteoblasts and evaluate cellular strain distributions. Ultramicroscopy. 86:85-95.
10. Chien, S., K. L. Sung, G. W. Schmid-Schonbein, R. Skalak, E. A. Schmalzer, and S. Usami. 1987. Rheology of leukocytes. Ann. N. Y. Acad. Sci. 516:333-347.
11. Clark, C. B., N. L. McKnight, and J. A. Frangos. 2002. Strain and strain rate activation of G proteins in human endothelial cells. Biochem. Biophys. Res. Commun. 299:258-262.
12. Davies, P. F. 1995. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519-560.
13. Dimova, R., C. Dietrich, A. Hadjiisky, K. Danov, and P. Pouligny. 1999. Falling ball viscosimetry of giant vesicle membranes: finite-size effects. Eur. Phys. J. B. 12:589-598.
14. Dong, C., and R. Skalak. 1992. Leukocyte deformability: finite element modeling of large viscoelastic deformation. J. Theor. Biol. 158:173-193.
15. Dong, C., R. Skalak, and K. L. Sung. 1991. Cytoplasmic rheology of passive neutrophils. Biorheology. 28:557-567.
16. Dong, C., R. Skalak, K. L. Sung, G. W. Schmid-Schonbein, and S. Chien. 1988. Passive deformation analysis of human leukocytes. J. Biomech. Eng. 110:27-36.
17. Evans, E. 1983. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipette aspiration tests. Biophys. J. 43:27-30.
18. Evans, E. 1989. B Structure and deformation properties of red blood cells: concepts and quantitative methods. Meth. Enzymol. 173:3-35.
19. Fabry, B., G. Maksym, J. Butler, M. Glogauer, D. Navajas, and J. Fredberg. 2001. Scaling the microrheology of living cells. Phys. Rev. Lett. 87: 148102.
20. Fabry, B., G. N. Maksym, S. A. Shore, P. E. Moore, R. A. Panettieri, Jr., J. P. Butler, and J. J. Fredberg. 2001. Signal transduction in smooth muscle, selected contribution: time course and heterogeneity of contractile responses in cultured human airway smooth muscle cells. J. Appl. Physiol. 91:986-994.
21. Glogauer, M., and J. Ferrier. 1998. A new method for application of force to cells via ferric oxide beads. Pflugers Arch. Eur. J. Physiol. 435:320-327.
22. Guilak, F., J. R. Tedrow, and R. Burgkart. 2000. Viscoelastic properties of the cell nucleus. Biochem. Biophys. Res. Commun. 269:781-786.
23. Gullingsrud, J., D. Kosztin, and K. Schulten. 2001. Structural determinants of MscL gating studied by molecular dynamics simulations. Biophys. J. 80:2074-2081.
24. Huang, H., C. Y. Dong, H.-S. Kwon, J. D. Sutin, R. D. Kamm, and P. T. C. So. 2002. Three-dimensional cellular deformation analysis with a two-photon magnetic manipulator workstation. Biophys. J. 82:2211-2223.
25. Hwang, W., and R. Waugh. 1997. Energy of dissociation of lipid bilayer from the membrane skeleton of red blood cells. Biophys. J. 72:2669-2678.
26. Ingber, D. E. 1997. Tensegrity: the architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 59:575-599.
27. Landau, L. D., and E. M. Lifschitz. 1988. Mechanics. Translated from the Russian by J. B. Sykes and J. S. Bell, Pergamon Press, New York.
28. Laurent, V., S. Henon, E. Planus, R. Fodil, M. Balland, D. Isabey, and F. Gallet. 2002. Assessment of mechanical properties of adherent living cells by bead micromanipulation: comparison of magnetic twisting cytometry vs. optical tweezers. J. Biomech. Eng. 124: 408-421.
29. Le Grimellec, C., E. Lesniewska, M.-C. Giocondi, E. Finot, V. Vie, and J.-P. Goudonnet. 1998. Imaging of the surface of living cells by low-force contact-mode atomic force microscopy. Biophys. J. 75:695-703.
30. Lodish, H., A. Berk, S. L. Zipursky, P. Matsudaira, D. Baltimore, and J. Darnell. 2000. Molecular Cell Biology. W.H. Freedman and Co., New York.
31. McVittie, A. 2001. Pathways for Mechanotransduction in Pressurized Airway Epithelial Cells. Massachusetts Institute of Technology, Cambridge, MA.
32. Mijailovich, S. M., M. Kojic, M. Zivkovic, B. Fabry, and J. J. Fredberg. 2002. A finite element model of cell deformation during magnetic bead twisting. J. Appl. Physiol. 93:1429-1436.
33. Ogden, R. W. 1984. Non-Linear Elastic Deformations, Chapt. 2. Prentice Hall, Chichester, England.
34. Resnick, N., and M. A. Gimbrone. 1995. Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 9:874-882.
35. Ressler, B., R. T. Lee, S. H. Randell, J. M. Drazen, and R. D. Kamm. 2000. Molecular responses of rat tracheal epithelial cells to transmembrane pressure. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L1264-L1272.
36. Sawada, Y., and M. P. Sheetz. 2002. Force transduction by Triton cytoskeletons. J. Cell Biol. 156:609-615.
37. Theret, D. P., M. J. Levesque, M. Sato, R. M. Nerem, and L. T. Wheeler. 1998. The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. J. Biomech. Eng. 110: 190-199.
38. Thoumine, O., and A. Ott. 1997. Timescale dependent viscoelastic and contractile regimes in fibroblasts probed by microplate manipulation. J. Cell Sci. 110:2109-2116.
39. Tran-Son-Tay, R., D. Needham, A. Yeung, and R. M. Hochmuth. 1991. Time-dependent recovery of passive neutrophils after large deformation. Biophys. J. 60:856-866.
40. Turner, M. S., and P. Sens. 1999. Inclusions on fluid membranes anchored to elastic media. Biophys. J. 76:564-572.
41. Wang, N., J. P. Butler, and D. E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1124-1127.
42. Yamada, S., D. Wirtz, and S. C. Kuo. 2000. Mechanics of living cells measured by laser tracking microrheology. Biophys. J. 78:1736-1747.
43. Zhelev, D., D. Needham, and R. Hochmuth. 1994. A novel micropipette method for measuring the bending modulus of vesicle membranes. Biophys. J. 67:720-727.
44. Zhu, C., G. Bao, and N. Wang. 2000. Cell mechanics: mechanical response, cell adhesion, and molecular deformation. Annu. Rev. Biomed. Eng. 2:189-226.