Viscoelastic properties of living embryonic tissues: a quantitative study.

A number of properties of certain living embryonic tissues can be explained by considering them as liquids. Tissue fragments left in a shaker bath round up to form spherical aggregates, as do liquid drops. When cells comprising two distinct embryonic tissues are mixed, typically a nucleation-like process takes place, and one tissue sorts out from the other. The equilibrium configurations at the end of such sorting out phenomena have been interpreted in terms of tissue surface tensions arising from the adhesive interactions between individual cells. In the present study we go beyond these equilibrium properties and study the viscoelastic behavior of a number of living embryonic tissues. Using a specifically designed apparatus, spherical cell aggregates are mechanically compressed and their viscoelastic response is followed. A generalized Kelvin model of viscoelasticity accurately describes the measured relaxation curves for each of the four tissues studied. Quantitative results are obtained for the characteristic relaxation times and elastic and viscous parameters. Our analysis demonstrates that the cell aggregates studied here, when subjected to mechanical deformations, relax as elastic materials on short time scales and as viscous liquids on long time scales.

[1]  N. Boccara,et al.  Dynamical Phenomena at Interfaces, Surfaces and Membranes , 1992 .

[2]  T. N. Stevenson,et al.  Fluid Mechanics , 2021, Nature.

[3]  H. Gaub,et al.  Viscoelastic moduli of sterically and chemically cross-linked actin networks in the dilute to semidilute regime: measurements by oscillating disk rheometer , 1991 .

[4]  H. M. Princen,et al.  The nonlinear elastic behavior of polydisperse hexagonal foams and concentrated emulsions , 1991 .

[5]  K. Heintzelman,et al.  Liquid-tissue behavior and differential cohesiveness during chick limb budding. , 1978, Journal of embryology and experimental morphology.

[6]  M. S. Steinberg,et al.  Two distinct adhesion mechanisms in embryonic neural retina cells. I. A kinetic analysis. , 1981, Developmental biology.

[7]  K. Zaner,et al.  Viscoelasticity of F-actin measured with magnetic microparticles , 1989, The Journal of cell biology.

[8]  James A. Glazier,et al.  Three-dimensional magnetic resonance imaging of a liquid foam , 1995 .

[9]  A. Sakanishi,et al.  Effects of viscoelasticity of cytoplasm on the complex viscosity of red blood cell suspensions. , 1988, Biorheology.

[10]  M. S. Steinberg,et al.  Embryonic tissues as elasticoviscous liquids. I. Rapid and slow shape changes in centrifuged cell aggregates. , 1978, Journal of cell science.

[11]  K. D. Pithia,et al.  Rheology of liquid foams , 1994 .

[12]  Michael Locke,et al.  Cellular membranes in development , 1964 .

[13]  E. Sackmann,et al.  Temperature-induced sol-gel transition and microgel formation in alpha -actinin cross-linked actin networks: A rheological study. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[14]  Malcolm S. Steinberg,et al.  Liquid behavior of embryonic tissues , 1982 .

[15]  M. S. Steinberg,et al.  Two distinct adhesion mechanisms in embryonic neural retina cells. II. An immunological analysis. , 1981, Developmental biology.

[16]  D. Reinelt,et al.  On the shearing flow of foams and concentrated emulsions , 1990, Journal of Fluid Mechanics.

[17]  H. M. Phillips Liquid-Tissue Mechanics in Amphibian Gastrulation: Germ-Layer Assembly in Rana Pipiens , 1978 .

[18]  Chen,et al.  Probing the structure of the cytoplasmic domain of the aspartate receptor by targeted disulfide cross-linking , 1997, Biochemistry.

[19]  Y. Hiramoto,et al.  Mechanical properties of the protoplasm of the sea urchin egg. I. Unfertilized egg. , 1969, Experimental cell research.

[20]  Glazier,et al.  Simulation of the differential adhesion driven rearrangement of biological cells. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[21]  P. Janmey,et al.  Mechanical properties of cytoskeletal polymers. , 1991, Current opinion in cell biology.

[22]  G. Forgacs,et al.  Surface tensions of embryonic tissues predict their mutual envelopment behavior. , 1996, Development.

[23]  J. P. Paul,et al.  Biomechanics , 1966 .

[24]  D. Taylor,et al.  Probing the structure of cytoplasm , 1986, The Journal of cell biology.

[25]  R. Bird Dynamics of Polymeric Liquids , 1977 .

[26]  D. Weaire,et al.  The effect of strain upon the topology of a soap froth , 1992 .

[27]  Malcolm S. Steinberg,et al.  Reconstruction of Tissues by Dissociated Cells , 1963 .

[28]  M. S. Steinberg,et al.  Do rates of intercellular adhesion measure the cell affinities reflected in cell-sorting and tissue-spreading configurations? , 1976, Developmental biology.

[29]  M. S. Steinberg,et al.  Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. , 1970, The Journal of experimental zoology.

[30]  P A Valberg,et al.  Cytoplasmic motions, rheology, and structure probed by a novel magnetic particle method , 1985, The Journal of cell biology.

[31]  H. M. Princen,et al.  Rheology of foams and highly concentrated emulsions , 1983 .

[32]  José C. M. Mombach,et al.  Quantitative comparison between differential adhesion models and cell sorting in the presence and absence of fluctuations. , 1995, Physical review letters.

[33]  D Needham,et al.  Viscosity of passive human neutrophils undergoing small deformations. , 1993, Biophysical journal.

[34]  M. S. Steinberg,et al.  Embryonic tissues as elasticoviscous liquids. II. Direct evidence for cell slippage in centrifuged aggregates. , 1977, Developmental biology.

[35]  Y. Hiramoto Observations and measurements of sea urchin eggs with a centrifuge microscope , 1967, Journal of the American Veterinary Medical Association.

[36]  J. Thomson,et al.  Two distinct adhesion mechanisms in embryonic neural retina cells. III. Functional specificity. , 1981, Developmental biology.

[37]  K Luby-Phelps,et al.  Viscoelastic response of fibroblasts to tension transmitted through adherens junctions. , 1997, Biophysical journal.

[38]  Malcolm S. Steinberg,et al.  The Problem of Adhesive Selectivity in Cellular Interactions , 1964 .

[39]  Y Hiramoto Mechanical properties of the protoplasm of the sea urchin egg. II. Fertilized egg. , 1969, Experimental cell research.

[40]  N S Goel,et al.  A rheological mechanism sufficient to explain the kinetics of cell sorting. , 1972, Journal of theoretical biology.

[41]  E. Sackmann,et al.  On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. , 1988, Biophysical journal.

[42]  Steinberg,et al.  Liquid properties of embryonic tissues: Measurement of interfacial tensions. , 1994, Physical review letters.

[43]  J. Folkman,et al.  Role of cell shape in growth control , 1978, Nature.

[44]  H. M. Princen,et al.  Rheology of foams and highly concentrated emulsions: IV. An experimental study of the shear viscosity and yield stress of concentrated emulsions , 1989 .

[45]  Studies of mechanical aspects of amoeboid locomotion. , 1993, Blood cells.