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PMID: 9591650 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Viscoelastic properties of living embryonic tissues: a quantitative study.

Biophysical journal ·Vol. 74 ·No. 5 ·1998-05-00 ·Pages 2227-34

Forgacs G, Foty RA, Shafrir Y, Steinberg MS

Abstract

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.

MeSH Terms
Animals Cell Aggregation Chick Embryo/physiology Elasticity Heart/embryology Kinetics Limb Buds/physiology Liver/embryology,physiology Models, Biological Myocardial Contraction Retina/embryology Viscosity
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Forgacs G
Department of Physics and Biology, Clarkson University, Potsdam, New York 13699-5820, USA. forgacs@polaris.clarkson.edu
Foty R A
Shafrir Y
Steinberg M S
References (24)
24 references, click to expand
  1. Cytoplasmic motions, rheology, and structure probed by a novel magnetic particle method.
    J Cell Biol. 1985 Jul;101(1):130-40 PMID: 4040136
  2. Temperature-induced sol-gel transition and microgel formation in alpha -actinin cross-linked actin networks: A rheological study.
    Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1996 Aug;54(2):1802-1810 PMID: 9965260
  3. Do rates of intercellular adhesion measure the cell affinities reflected in cell-sorting and tissue-spreading configurations?
    Dev Biol. 1976 Sep;52(2):246-62 PMID: 12194436
  4. Liquid properties of embryonic tissues: Measurement of interfacial tensions.
    Phys Rev Lett. 1994 Apr 4;72(14):2298-2301 PMID: 10055839
  5. Two distinct adhesion mechanisms in embryonic neural retina cells. I. A kinetic analysis.
    Dev Biol. 1981 Jan 15;81(1):96-105 PMID: 6780398
  6. Liquid-tissue behavior and differential cohesiveness during chick limb budding.
    J Embryol Exp Morphol. 1978 Oct;47:1-15 PMID: 722227
  7. Role of cell shape in growth control.
    Nature. 1978 Jun 1;273(5661):345-9 PMID: 661946
  8. Studies of mechanical aspects of amoeboid locomotion.
    Blood Cells. 1993;19(2):375-86; discussion 386-8 PMID: 8312570
  9. Viscosity of passive human neutrophils undergoing small deformations.
    Biophys J. 1993 May;64(5):1596-601 PMID: 8324194
  10. Surface tensions of embryonic tissues predict their mutual envelopment behavior.
    Development. 1996 May;122(5):1611-20 PMID: 8625847
  11. Embryonic tissues as elasticoviscous liquids. II. Direct evidence for cell slippage in centrifuged aggregates.
    Dev Biol. 1977 Sep;59(2):124-34 PMID: 561007
  12. Viscoelastic response of fibroblasts to tension transmitted through adherens junctions.
    Biophys J. 1997 Nov;73(5):2798-808 PMID: 9370474
  13. Embryonic tissues as elasticoviscous liquids. I. Rapid and slow shape changes in centrifuged cell aggregates.
    J Cell Sci. 1978 Apr;30:1-20 PMID: 649680
  14. A rheological mechanism sufficient to explain the kinetics of cell sorting.
    J Theor Biol. 1972 Oct;37(1):43-73 PMID: 4652421
  15. Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation.
    Science. 1963 Aug 2;141(3579):401-8 PMID: 13983728
  16. Quantitative comparison between differential adhesion models and cell sorting in the presence and absence of fluctuations.
    Phys Rev Lett. 1995 Sep 11;75(11):2244-2247 PMID: 10059250
  17. Effects of viscoelasticity of cytoplasm on the complex viscosity of red blood cell suspensions.
    Biorheology. 1988;25(1-2):123-8 PMID: 3196808
  18. Probing the structure of cytoplasm.
    J Cell Biol. 1986 Jun;102(6):2015-22 PMID: 2423529
  19. Mechanical properties of cytoskeletal polymers.
    Curr Opin Cell Biol. 1991 Feb;3(1):4-11 PMID: 1854482
  20. Simulation of the differential adhesion driven rearrangement of biological cells.
    Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1993 Mar;47(3):2128-2154 PMID: 9960234
  21. On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields.
    Biophys J. 1988 Sep;54(3):495-508 PMID: 3207837
  22. Viscoelasticity of F-actin measured with magnetic microparticles.
    J Cell Biol. 1989 Nov;109(5):2233-43 PMID: 2808527
  23. 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. 1970 Apr;173(4):395-433 PMID: 5429514
  24. Mechanical properties of the protoplasm of the sea urchin egg. I. Unfertilized egg.
    Exp Cell Res. 1969 Aug;56(2):201-8 PMID: 5387908
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1998-05-00
Pages
2227-34
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1299566
Subset
IM
Grants
NIGMS NIH HHS · GM52009 · United States
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