Surface tensions of embryonic tissues predict their mutual envelopment behavior.

During embryonic development, certain tissues stream to their destinations by liquidlike spreading movements. According to the 'differential adhesion hypothesis', these movements are guided by cell-adhesion-generated tissue surface tensions (sigmas), operating in the same manner as surface tensions do in the mutual spreading behavior of immiscible liquids, among which the liquid of lower surface tension is always the one that spreads over its partner. In order to conduct a direct physical test of the 'differential adhesion hypothesis', we have measured the sigmas of aggregates of five chick embryonic tissues, using a parallel plate compression apparatus specifically designed for this purpose, and compared the measured values with these tissues' mutual spreading behaviors. We show that aggregates of each of these tissues behave for a time as elasticoviscous liquids with characteristic surface tension values. Chick embryonic limb bud mesoderm (sigma = 20.1 dyne/cm) is enveloped by pigmented epithelium (sigma = 12.6 dyne/cm) which, in turn, is enveloped by heart (sigma = 8.5 dyne/cm) which, in turn, is enveloped by liver (sigma = 4.6 dyne/cm) which, in turn, is enveloped by neural retina (sigma = 1.6 dyne/cm). Thus, as predicted, the tissues' surface tension values fall in the precise sequence required to account for their mutual envelopment behavior.

[1]  D. Fristrom,et al.  The making of a fly leg: A model for epithelial morphogenesis , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[3]  M. Yoneda.  TENSION AT THE SURFACE OF SEA-URCHIN EGG: A CRITICAL EXAMINATION OF COLE'S EXPERIMENT. , 1964, The Journal of experimental biology.

[4]  Philip L. Townes,et al.  Directed movements and selective adhesion of embryonic amphibian cells , 1955 .

[5]  G. S. Davis.  Migration-Directing Liquid Properties of Embryonic Amphibian Tissues , 1984 .

[6]  G. Schoenwolf.  Formation and patterning of the avian neuraxis: one dozen hypotheses. , 1994, Ciba Foundation symposium.

[7]  A. Harris,et al.  Increased contractile strength and tightened adhesions to the substratum result from reverse transformation of CHO cells by dibutyryl cyclic adenosine monophosphate. , 1983, Journal of cell science.

[8]  M. S. Steinberg,et al.  Experimental modulation of intercellular cohesiveness: reversal of tissue assembly patterns. , 1972, Developmental biology.

[9]  M. Tessier-Lavigne,et al.  Guidance and induction of branch formation in developing axons by target-derived diffusible factors , 1995, Current Opinion in Neurobiology.

[10]  M S Steinberg.  Cell-cell recognition in multicellular assembly: levels of specificity. , 1978, Symposia of the Society for Experimental Biology.

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

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

[13]  John S. Rowlinson,et al.  Molecular Theory of Capillarity , 1983 .

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

[15]  B. J. Winer.  Statistical Principles in Experimental Design , 1992 .

[16]  M. S. Steinberg,et al.  Mechanism of Tissue Reconstruction by Dissociated Cells, II: Time-Course of Events , 1962, Science.

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

[18]  M. Collins.  Electrokinetic properties of dissociated chick embryo cells. Calcium ion binding by neural retinal cells. , 1966, The Journal of experimental zoology.

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

[20]  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.

[21]  M. Takeichi,et al.  Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[22]  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.

[23]  L. Kornberg,et al.  Signal transduction by cell adhesion receptors. , 1995, Biochimica et biophysica acta.

[24]  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.

[25]  C. Ettensohn,et al.  Mechanisms of Epithelial Invagination , 1985, The Quarterly Review of Biology.

[26]  P. Taylor,et al.  Physical chemistry of surfaces , 1991 .

[27]  M. S. Steinberg,et al.  Equilibrium measurements of embryonic chick cell adhesiveness. I. Shape equilibrium in centrifugal fields. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Steinberg Ms,et al.  Cell-cell recognition in multicellular assembly: levels of specificity. , 1978 .

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

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

[31]  M. S. Steinberg,et al.  ON THE MECHANISM OF TISSUE RECONSTRUCTION BY DISSOCIATED CELLS, III. FREE ENERGY RELATIONS AND THE REORGANIZATION OF FUSED, HETERONOMIC TISSUE FRAGMENTS. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[34]  J. Trinkaus,et al.  DIFFERENTIATION IN CULTURE OF MIXED AGGREGATES OF DISSOCIATED TISSUE CELLS. , 1955, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. S. Steinberg,et al.  On the mechanism of tissue reconstruction by dissociated cells. I. Population kinetics, differential adhesiveness. and the absence of directed migration. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Leptin.  Morphogenesis: Control of epithelial cell shape changes , 1994, Current Biology.

[37]  W. Barry,et al.  Mechanisms of transmembrane calcium movement in cultured chick embryo ventricular cells , 1982, The Journal of physiology.