Do rates of intercellular adhesion measure the cell affinities reflected in cell-sorting and tissue-spreading configurations?

Moyer, Wayne A.; Steinberg, Malcolm S.

doi:10.1016/0012-1606(76)90244-x

Cited by 30 publications

(6 citation statements)

References 26 publications

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“…Interpretations of this force must consider that the plane of separation may not be defined and that such factors as the plasticity of the adhering surfaces and the rate of application of the distractive force can greatly affect the peak ‘force of distraction’ . Kinetic measurements reflect the rate of initiation of adhesions. The utility of kinetic measurements is restricted by the facts that forward reaction rates, including the rate of cell aggregation in stirred suspensions, are limited not by free energies of reaction but by activation energies.…”

Section: Differential Adhesion Definedmentioning

confidence: 99%

Differential adhesion in model systems

Foty

Steinberg

2013

WIREs Developmental Biology

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During embryonic development, cells or groups of cells migrate from their locations of origin to assume their correct anatomical positions. Intercellular adhesion plays an active and instructive role in orchestrating this process. Precisely how adhesion provides spatial positioning information is a subject of intense interest. In the 1960s, Steinberg proposed the differential adhesion hypothesis (DAH) to explain how differences in the intensity of cell adhesion could give rise to predictable spatial interactions between different cell types. The DAH is grounded in the same set of physical principles governing the interaction of immiscible fluids and thus provides a rigorous conceptual framework connecting the chemistry of cell adhesion to the physics underlying cell and tissue segregation. Testing the DAH required the development of methods to measure intercellular cohesion and of assays to accurately assess relative spatial position between cells. The DAH has been experimentally verified and computationally simulated. Moreover, evidence concerning the role of differential adhesion in a number of morphodynamic events is accumulating. It is clear that differential adhesion is a major driving force in various aspects of embryonic development, but recent studies have also advanced the concept that other factors, such as cortical tension and elasticity, may also be involved in fine tuning, or even driving the process. It is likely that an interplay between adhesion and these other factors co-operate to generate the forces required for tissue self-organization.

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Section: Differential Adhesion Definedmentioning

confidence: 99%

Differential adhesion in model systems

Foty

Steinberg

2013

WIREs Developmental Biology

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“…One of us has written extensively about this (Duguay et al, 2003, Moyer and Steinberg 1976, Steinberg 1970, Steinberg 1975, Steinberg 1978b, Steinberg 1996) but here we wish only to note what we regard as the underlying causes. The DAH arose from the first experiments designed to discriminate among three competing explanations for the reorganizational behavior Holtfreter categorized under the rubric of "tissue affinities" (Holtfreter 1939, Townes andHoltfreter 1955).…”

Section: Tissue Segregation: Of Theories and Measurementsmentioning

confidence: 99%

“…This measurement of binding rates with the intention to quantify binding energies was physically unsupportable (Moyer andSteinberg 1976, Steinberg 1970). Nevertheless, it found favor among cell and developmental biologists little engaged with physics but thoroughly steeped in the biochemical specificities of antigen-antibody and enzyme-substrate reactions because the cells were found to bind to aggregates of like cells faster than to those of unlike cells.…”

Section: Tissue Segregation: Of Theories and Measurementsmentioning

confidence: 99%

Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy

Foty¹,

Steinberg²

2004

Int. J. Dev. Biol.

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185

151

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We review evidence concerning the basis for tissue segregation during embryonic development. This compartmentalization is shown to be an immiscibility phenomenon caused by changes in the strengths of adhesions between mobile cells which accompany their differentiation and generate interfacial tensions at cell population boundaries. The mobile cells exchange neighbors in response to these adhesion-generated forces which impel the system toward the configuration of maximal binding. Cadherins dominate these intercellular adhesions, but integrin-fibronectinbased adhesions also contribute to them as well as to cell-matrix adhesions. At the interface between two segregating cell populations are three kinds of cell-cell interfaces: a-a, b-b and a-b. Tissue immiscibility (segregation) results when the cross-adhesion is weaker than the mean value of the two kinds of self-adhesions, does not require (although it permits) qualitative changes in cell adhesion molecules and is easily generated even by moderate changes in the quantities of adhesion molecules on the cell surfaces. All type I and II cadherins tested cross-adhere, in most cases with strengths close to those of their self-adhesions. Is malignant invasion a process of cell segregation in reverse, in which the cross-adhesion between cancer cells and host tissue components is strong relative to their self-adhesions? We review evidence for cadherin involvement in breast, prostate and brain cancers. Despite evidence that N-cadherin enhances the invasiveness of certain cancer cells, we have found that increasing the expression not only of functional E-cadherin but also of Por N-cadherin restrains the spreading of other malignant cell lines over (and through) a reconstituted extracellular matrix.

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“…Aggregation rates (Roth and Weston, 1967;Roth, 1968;Nose et al, 1988) are only reflective of the initiation of adhesions between suspended cells. Such measurements present at least three obstacles to their use to measure intercellular binding energy: (1) the rate of initial cell attachment cannot measure the strengths of mature, physiologically relevant adhesions (Moyer and Steinberg, 1976); (2) rate processes are limited not by the specific free energy of reaction (in this case the strength of adhesion) but by entirely unrelated activation energies (Glasstone et al, 1941); (3) the shear force used in comparing the aggregation rates of different cell populations may itself create the functional equivalent of an activation energy barrier preventing the aggregation of one population of mutually adhesive cells while permitting that of another and thus creating a misleading impression of adhesive specificity (Duguay et al, 2003). To rigorously measure intercellular binding energy, measurements rooted in thermodynamics must be used.…”

Section: Introductionmentioning

confidence: 99%

Tissue surface tensions guide in vitro self‐assembly of rodent pancreatic islet cells

Jia

DaJusta

Foty

2007

Developmental Dynamics

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The organization of endocrine cells in pancreatic islets is established through a series of morphogenetic events involving cell sorting, migration, and re-aggregation processes for which intercellular adhesion is thought to play a central role. In animals, these morphogenetic events result in an islet topology in which insulin-secreting cells form the core, while glucagon, somatostatin, and pancreatic polypeptide-secreting cells segregate to the periphery. Isolated pancreatic islet cells self-assemble in vitro into pseudoislets with the same cell type organization as native islets. It is widely held that differential adhesion between cells of the pancreatic islets generates this specific topology. However, this differential adhesion has never been rigorously quantified. In this manuscript, we use tissue surface tensiometry to measure the cohesivity of spherical aggregates from three immortalized mouse pancreatic islet cell lines. We show that, as predicted by the differential adhesion hypothesis, aggregates of the internally segregating INS-1 and MIN6 beta-cell lines are substantially more cohesive than those of the externally segregating ␣-TC line. Furthermore, we show that forced overexpression of P-cadherin by ␣-TC cells significantly perturbs the sorting process. Collectively, the data indicate that differential adhesion can drive the in vitro organization of immortalized rodent pancreatic islet cells.

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Do rates of intercellular adhesion measure the cell affinities reflected in cell-sorting and tissue-spreading configurations?

Cited by 30 publications

References 26 publications

Differential adhesion in model systems

Differential adhesion in model systems

Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy

Tissue surface tensions guide in vitro self‐assembly of rodent pancreatic islet cells

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