A prestressed cable network model of the adherent cell cytoskeleton

Biophysical Journal

Volumn 84, Issue 2 I, 2003, Pages 1328-1336

  Coughlin, Mark F ^a,c   Stamenović, Dimitrije ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Boston University   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL STRUCTURE; CYTOMETRY; CYTOSKELETON; MATHEMATICAL ANALYSIS; MEASUREMENT; MOLECULAR MODEL; SIMULATION;

EID: 0037305872     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74948-0     Document Type: Article

References (43)

1. Amos, L. A., and W. B. Amos. 1991. Molecules of the Cytoskeleton. The Guilford Press, New York.
2. 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.
3. 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.
4. Cai, S., L. Pestic-Dragovich, M. E. O'Donnell, N. Wang, D. E. Ingber, E. Elson, and P. De Lanerolle. 1998. Regulation of cytoskeletal mechanics and cell growth by myosin light chain phosphorylation. Am. J. Physiol. 275:C1349-C1356.
5. Caille, N., Y. Tardy, and J. J. Meister. 1998. Assessment of strain field in endothelial cells subjected to uniaxial deformation of their substrate. Ann. Biomed. Eng. 26:409-416.
6. Chen, C. S., M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber. 1997. Geometric control of cell life and death. Science. 276:1425-1428.
7. Chicurel, M. E., C. S. Chen, and D. E. Ingber. 1998. Cellular control lies in the balance of forces. Curr. Opin. Cell Biol. 10:232-239.
8. Coughlin, M. F. 2000. The Microstructural Basis of Cellular Deformability. Dissertation, Department of Biomedical Engineering, Boston University, Boston.
9. Coughlin, M. F., and D. Stamenović. 1997. A tensegrity structure with buckling compression elements: applications to cell mechanics. J. Appl. Mech. 64:480-486.
10. Coughlin, M. F., and D. Stamenović. 1998. A tensegrity model of the cytoskeleton in spread and round cells. J. Biomech. Eng. 120:770-777.
11. Discher, D. E., D. H. Boal, and S. K. Boey. 1998. Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys. J. 75:1584-1597.
12. Elson, E. L. 1988. Cellular mechanics as an indicator of cytoskeletal structure and function. In Annual Review of Biophysics and Biophysical Chemistry. D. M. Engelman, C. R. Cantor, and T. D. Pollard, editors. Annual Reviews Inc., Palo Alto. 397-430.
13. Elson, E. L., B. B. Daily, W. B. McConnaughey, C. Pastemak, and N. O. Petersen. 1983. Measurement of forces which determine the shapes of adherent cells in culture. In Frontiers in Biochemical and Biophysical Studies of Proteins and Membranes. T.-Y. Liu, S. Sakakibara, A. N. Schechter, K. Yagi, K. Yajima, and K. T. Yasunobu, editors. Elsevier Science Publishing Co., Inc., New York. 399-411.
14. Fabry, B., G. N. Maksym, J. P. Butler, M. Glogauer, D. Navajas, and J. J. Fredberg. 2001. Scaling the microrheology of living cells. Phys. Rev. Lett. 87:148102.
15. Folkman, J., and A. Mascona. 1978. Role of cell shape in growth control. Nature. 273:345-349.
16. Gerald, C. F., and P. O. Wheatley. 1989. Applied Numerical Analysis. Addison-Wesley Publishing Company, Inc., Reading.
17. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923-934.
18. Hansen, J. C., R. Skalak, S. Chien, and A. Hoger. 1996. An elastic network model based on the structure of the red blood cell membrane skeleton. Biophys. J. 70:146-166.
19. Hansen, J. C., R. Skalak, S. Chien, and A. Hoger. 1997. Influence of network topology on the elasticity of the red blood cell membrane skeleton. Biophys. J. 72:2369-2381.
20. Hubmayr, R. D., S. A. Shore, J. J. Fredberg, E. Planus, R. A. Panettieri, W. Moller, J. Heyder, and N. Wang. 1996. Pharmacological activation changes stiffness of cultured human airway smooth muscle cells. Am. J. Physiol. 271:C1660-C1668.
21. Janmey, P. A. 1996. Coping with cellular stress: the mechanical resistance of porous protein networks. Biophys. J. 71:3-5.
22. Janmey, P. A. 1998. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol. Rev. 78:763-781.
23. Kishino, A., and T. Yanagida. 1988. Force measurements by micromanipulation of a single actin filament by glass needles. Nature. 334:74-76.
24. Kojima, H., A. Ishijima, and T. Yanagida. 1994. Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc. Natl. Acad. Sci. USA. 91:12962-12966.
25. Luby-Phelps, K., D. L. Taylor, and F. Lanni. 1986. Probing the structure of cytoplasm. J. Cell Biol. 102:2015-2022.
26. Maksym, G. N., B. Fabry, J. P. Butler, D. Navajas, D. J. Tschumperlin, J. D. Laporte, and J. J. Fredberg. 2000. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. J. Appl. Physiol. 89:1619-1632.
27. McConnaughey, W. B., and N. O. Petersen. 1980. Cell poker: an apparatus for stress-strain measurements on living cells. Rev. Sci. Instrum. 51:575-580.
28. Petersen, N. O., W. B. McConnaughey, and E. L. Elson. 1981. Investigations of structural determinants of cell shape. Comm. Molec. Cell. Biophys. 1:135-147.
29. Petersen, N. O., W. B. McConnaughey, and E. L. Elson. 1982. Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B. Proc. Natl. Acad. Sci. USA. 79:5327-5331.
30. Pourati, J., A. Maniotis, D. Spiegel, J. L. Schaffer, J. P. Butler, J. J. Fredberg, D. E. Ingber, D. Stamenović, and N. Wang. 1998. Is cytoskeletal tension a major determinant of cell deformability in adherent endothelial cells? Am. J. Physiol. 274:C1283-C1289.
31. Satcher, R., C. F. Dewey, Jr., and J. H. Hartwig. 1997. Mechanical remodeling of the endothelial surface and actin cytoskeleton induced by fluid flow. Microcirculation. 4:439-453.
32. Shroff, S. G., D. R. Saner, and R. Lal. 1995. Dynamic micromechanical properties of cultured rat atrial myocytes measured by atomic force microscopy. Am. J. Physiol. 269:C286-C292.
33. Singhvi, R., A. Kumar, G. P. Lopez, G. N. Stephanopoulos, D. I. C. Wang, G. M. Whitesides, and D. E. Ingber. 1994. Engineering cell shape and function. Science. 264:696-698.
34. Sokolnikoff, I. S. 1946. Mathematical Theory of Elasticity. Krieger Publishing Company, Malabar.
35. Stamenović, D., and M. F. Coughlin. 2000. A quantitative model of cellular elasticity based on tensegrity. J. Biomech. Eng. 122:39-43.
36. Stamenović, D., and M. F. Coughlin. 1999b. The role of prestress and architecture of the cytoskeleton and deformability of cytoskeletal filaments in mechanics of adherent cells: a quantitative study. J. Theor. Biol. 201:63-74.
37. Stamenović, D., J. J. Fredberg, N. Wang, J. P. Butler, and D. E. Ingber. 1996. A microstructural approach to cytoskeletal mechanics based on tensegrity. J. Theor. Biol. 181:125-136.
38. Stamenović, D., and N. Wang. 2000. Cellular responses to mechanical stress: engineering approaches to cytoskeletal mechanics. J. Appl. Physiol. 89:2085-2090.
39. Tsuda, Y., H. Yasutake, A. Ishijima, and T. Yanagida. 1996. Torsional rigidity of single actin filaments and actin-actin bond breaking force under torsion measured directly by in vitro micromanipulation. Proc. Natl. Acad. Sci. USA. 93:12937-12942.
40. Wang, N., J. P. Butler, and D. E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260:1124-1127.
41. Wang, N., and D. E. Ingber. 1994. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66:2181-2189.
42. Zahalak, G. I., W. B. McConnaughey, and E. L. Elson. 1990. Determination of cellular mechanical properties by cell poking, with an application to leukocytes. J. Biomech. Eng. 112:283-294.
43. Zhelev, D. V., D. Needham, and R. M. Hochmuth. 1994. Role of the membrane cortex in neutrophil deformation in small pipettes. Biophys. J. 67:696-705.