Viscoelastic properties of living embryonic tissues: A quantitative study

Biophysical Journal

Volumn 74, Issue 5, 1998, Pages 2227-2234

  Forgacs, Gabor ^a   Foty, Ramsey A ^b   Shafrir, Yinon ^a   Steinberg, Malcolm S ^b  

^a CLARKSON UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CHICK EMBRYO; EMBRYO; EMBRYONAL TISSUE; HEART VENTRICLE; LIMB BUD; LIVER; NONHUMAN; RETINA; VISCOELASTICITY;

ANIMALIA;

EID: 0031956939     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77932-9     Document Type: Article

References (40)

1. Byrd, B. R., R. C. Armstrong, and O. Hassager, 1977. Dynamics of Polymeric Liquids. John Wiley & Sons, New York.
2. Engelhardt, H., and E. Sackmann. 1988. On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. Biophys. J. 54: 495-508.
3. Folkman, J., and A. Moscona. 1978. Role of cell shape in growth control. Nature. 273:345-349.
4. Foty, R. A., G. Forgacs, C. M. Pfleger, and M. S. Steinberg. 1994. Liquid properties of embryonic tissues: measurement of interfacial tensions. Phys. Rev. Lett. 72:2298-2301.
5. Foty, R. A., C. M. Pfleger, G. Forgacs, and M. S. Steinberg. 1996. Surface tensions of embryonic tissues predict their envelopment behavior. Development. 122:1611-1620.
6. Fung, Y. C. 1993. Biomechanics. Springer-Verlag, New York.
7. Glazier, J. A., and F. Graner. 1993. Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E47:2128-2154.
8. Gordon, R., N. S. Goel, M. S. Steinberg, and L. L. Wiseman. 1972. A rheological mechanism sufficient to explain the kinetics of cell sorting. J. Theor. Biol. 37:43-73.
9. Heintzelman, K. F., H. M. Phillips, and G. S. Davis. 1978. Liquid-tissue behavior and differential cohesiveness during chick limb budding. J. Embryol. Exp. Morphol. 47:1-15.
10. Hiramoto, Y. 1968. Observation and measurements of sea urchin eggs with a centrifuge microscope. J. Cell Physiol. 69:219-230.
11. Hiramoto, Y. 1969. Mechanical properties of the protoplasm of the sea urchin egg. Exp. Cell Res. 56:201-208.
12. Hochmuth, R. M., H. P. Ting-Beal, B. B. Beaty, D. Needham, and R. Tran-Son-Tay. 1993. Viscosity of passive human neutrophils undergoing small deformations. Biophys. J. 64:1596-1601.
13. Janmey, P. A. 1991. Mechanical properties of cytoskeletal polymers. Curr. Opin. Cell Biol. 2:4-11.
14. Jay, P. Y., C. Pasternak, and E. L. Elson. 1993. Studies of aspects of amoeboid locomotion. Blood Cells. 19:375-386.
15. Kraynik, A. M. 1988. Foam flows. Annu. Rev. Fluid. Mech. 20:325-357.
16. Kraynik, A. M., D. A. Reinelt, and H. M. Princen. 1991. The nonlinear elastic behavior of polydisperse hexagonal foams and concentrated emulsions. J. Rheology. 35:1235-1253.
17. Landau, L. D., and E. M. Lifshitz. 1978. Fluid Mechanics. Pergamon Press, New York.
18. Luby-Phelps, K., D. L. Taylor, and F. Lanni. 1986. Probing the structure of the cytoplasm. J. Cell Biol. 102:2015-2022.
19. Mombach, J. C. M., J. A. Glazier, R. C. Raphael, and M. Zajac. 1995. Quantitative comparison between differential adhesion models and cell sorting in the presence and absence of fluctuations. Phys. Rev. Lett. 75:2244-2247.
20. Moyer, W. A., and M. S. Steinberg. 1976. Do rates of intercellular adhesion measure the cell affinities reflected in cell-sorting and tissue spreading configurations? Dev. Biol. 52:246-262.
21. Müller, O., H. E. Gaub, M. Bärmann, and E. Sackmann. 1991. Viscoelastic moduli of sterically and chemically cross-linked actin networks in dilute to semidilute regime: measurements by an oscillating disc rheometer. Macromolecules. 24:3111-3120.
22. Phillips, H. M., and G. S. Davis. 1978. Liquid-tissue mechanics in amphibian gastrulation: germ-layer assembly in Rana pipiens. Am. Zool. 18:81-93.
23. Phillips, H. M., and M. S. Steinberg. 1978. Embryonic tissues as elasticoviscous liquids: I. Rapid and slow shape changes in centrifuged cell aggregates. J. Cell Sci. 30:1-20.
24. Phillips, H. M., M. S. Steinberg, and B. H. Lipton. 1977. Embryonic tissues as elasticoviscous liquids: II. Direct morphological evidence for cell slippage in centrifuged aggregates. Dev. Biol. 59:124-134.
25. Pithia, K. D., and S. F. Edwards. 1994. Rheology of liquid foams. Physica. A205:565-576.
26. Prause, B. A., J. A. Glazier, S. J. Gravina, and C. D. Montemagno. 1995. Three dimensional magnetic resonance imaging of a liquid foam. J. Phys. Cond. Matt. 7:L511-L516.
27. Princen, H. M., and A. D. Kiss. 1989. Rheology of foams and highly concentrated emulsions: IV. An experimental study of the shear viscosity and yield stress of concentrated emulsions. J. Colloid Interface Sci. 128:176-187.
28. Ragsdale, G. K., J. Phelps, and K. Luby-Phelps. 1997. Viscoelastic response of fibroblasts to tension transmitted through adherens junctions. Biophys. J. 73:2798-2808.
29. Reinelt, D. A., and A. M. Kraynik. 1990. On the shearing flow of foams and concentrated emulsions. J. Fluid. Mech. 215:431-455.
30. Sakanishi, T. Y. 1988. Effects of viscoelasticity of cytoplasm on the complex viscosity of red blood cell suspensions. Biorheology. 25: 123-128.
31. Steinberg, M. S. 1963. Reconstruction of tissues by dissociated cells. Science. 141:401-408.
32. Steinberg, M. S. 1964. The problem of adhesive selectivity in cellular interactions. In Cellular Membranes in Development. M. Locke, editor. Academic Press, New York. 321-366.
33. Steinberg, M. S. 1970. Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J. Exp. Zool. 173:395-434.
34. Steinberg, M. S. 1993. The assembly of embryonic cells into tissues and organs mimics liquid behavior and is guided by interfacial energies arising from cellular adhesive interactions. In Dynamical Phenomena at Interfaces, Surfaces and Membranes. D. Beysens, N. Boccara, and G. Forgacs, editors. Nova Science Publishers, Commack, New York. 3-10.
35. Steinberg, M. S., and T. J. Poole. 1982. Liquid behavior of embryonic tissues. In Cell Behaviour. R. Bellairs, A. S. G. Curtis, and G. Dunn, editors. Cambridge University Press, Cambridge. 583-607.
36. Tempel, M., G. Isenberg, and E. Sackmann. 1996. Temperature-induced sol-gel transition and microgel formation in α-actinin cross-linked actin networks: a rheological study. Phys. Rev. E54:1802-1810.
37. Thomas, W. A., and M. S. Steinberg. 1981. Two distinct adhesion mechanisms in embryonic neural retina cells: I. A kinetic analysis. Dev. Biol. 81:96-105.
38. Valberg, P. A., and D. F. Albertini. 1985. Cytoplasmic motions, rheology and structure probed by a novel magnetic particle method. J. Cell Biol. 101:130-140.
39. Weaire, D., F. Bolton, and T. Herdtle. 1992. The effect of strain upon the topology of soap froth. Phil. Mag. Lett. 66:293-299.
40. Zaner, K. S., and P. A. Valberg. 1989. Viscoelasticity of F-actin measured with magnetic microparticles. J. Cell Biol. 109:2233-2243.