On the evolution of morphogenetic models: mechano-chemical interactions and an integrated view of cell differentiation, growth, pattern formation and morphogenesis

Authors

  • Séverine Urdy

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    1. Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid Strasse 4, CH-8006 Zurich, Switzerland
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    • Present address: Netherlands Institute for Systems Biology and CWI (Center for Mathematics and Computer Science), Science Park 123, 1098 XG Amsterdam, The Netherlands.


(E-mail: urdy@cwi.nl)

Abstract

In the 1950s, embryology was conceptualized as four relatively independent problems: cell differentiation, growth, pattern formation and morphogenesis. The mechanisms underlying the first three traditionally have been viewed as being chemical in nature, whereas those underlying morphogenesis have usually been discussed in terms of mechanics. Often, morphogenesis and its mechanical processes have been regarded as subordinate to chemical ones.

However, a growing body of evidence indicates that the biomechanics of cells and tissues affect in striking ways those phenomena often thought of as mainly under the control of cell-cell signalling. This accumulation of data has led to a revival of the mechano-transduction concept in particular, and of complexity in general, causing us now to consider whether we should retain the traditional conceptualization of development.

The researchers' semantic preferences for the terms ‘patterning’, ‘pattern formation’ or ‘morphogenesis’ can be used to describe three main ‘schools of thought' which emerged in the late 1970s. In the ‘molecular school’, the term patterning is deeply tied to the positional information concept. In the ‘chemical school’, the term ‘pattern formation’ regularly implies reaction-diffusion models. In the ‘mechanical school’, the term ‘morphogenesis’ is more frequently used in relation to mechanical instabilities. Major differences among these three schools pertain to the concept of self-organization, and models can be classified as morphostatic or morphodynamic. Various examples illustrate the distorted picture that arises from the distinction among differentiation, growth, pattern formation and morphogenesis, based on the idea that the underlying mechanisms are respectively chemical or mechanical.

Emerging quantitative approaches integrate the concepts and methods of complex sciences and emphasize the interplay between hierarchical levels of organization via mechano-chemical interactions. They draw upon recent improvements in mathematical and numerical morphogenetic models and upon considerable progress in collecting new quantitative data. This review highlights a variety of such models, which exhibit important advances, such as hybrid, stochastic and multiscale simulations.

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