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Programmed and self-organized flow of information during morphogenesis

Abstract

How the shape of embryos and organs emerges during development is a fundamental question that has fascinated scientists for centuries. Tissue dynamics arise from a small set of cell behaviours, including shape changes, cell contact remodelling, cell migration, cell division and cell extrusion. These behaviours require control over cell mechanics, namely active stresses associated with protrusive, contractile and adhesive forces, and hydrostatic pressure, as well as material properties of cells that dictate how cells respond to active stresses. In this Review, we address how cell mechanics and the associated cell behaviours are robustly organized in space and time during tissue morphogenesis. We first outline how not only gene expression and the resulting biochemical cues, but also mechanics and geometry act as sources of morphogenetic information to ultimately define the time and length scales of the cell behaviours driving morphogenesis. Next, we present two idealized modes of how this information flows — how it is read out and translated into a biological effect — during morphogenesis. The first, akin to a programme, follows deterministic rules and is hierarchical. The second follows the principles of self-organization, which rests on statistical rules characterizing the system’s composition and configuration, local interactions and feedback. We discuss the contribution of these two modes to the mechanisms of four very general classes of tissue deformation, namely tissue folding and invagination, tissue flow and extension, tissue hollowing and, finally, tissue branching. Overall, we suggest a conceptual framework for understanding morphogenetic information that encapsulates genetics and biochemistry as well as mechanics and geometry as information modules, and the interplay of deterministic and self-organized mechanisms of their deployment, thereby diverging considerably from the traditional notion that shape is fully encoded and determined by genes.

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Fig. 1: Programme versus self-organization in the flow of morphogenetic information.
Fig. 2: Polarized contractility drives tissue bending and invagination.
Fig. 3: Growth-driven mechanical instabilities drive tissue folding and looping.
Fig. 4: Tissue extension by programmed polarization of cellular active stresses.
Fig. 5: Impact of patterned boundaries and their geometry in tissue flows and extension.
Fig. 6: Mechanical and geometrical feedbacks control lumen formation to regulate tissue size and patterning.
Fig. 7: Morphogenesis of branched structures can be genetically programmed or emerge as self-organized.

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Acknowledgements

The authors thank all members of the Lecuit group for stimulating discussions and useful feedback on this manuscript. This review emerged from a lecture series at the Collège de France in 2018. The lab is supported by the ERC grant SelfControl #788308 and the Ligue contre le Cancer. C.C. is supported by the CNRS and T.L. by the Collège de France.

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Glossary

Denticles

Small cuticular bristles on the ventral side of Drosophila melanogaster larvae that are used for locomotion.

Strain

A measure of deformation of an object with respect to a reference length upon application of a mechanical stress. This is a dimensionless parameter

Reaction–diffusion systems

Mathematical models describing the change in space and time of the concentration of one or more chemical substances. They typically consider local chemical reactions producing or consuming chemical species and their diffusion.

Turing instabilities

A reaction–diffusion system in which the homogeneous equilibrium of mixed chemical substances is unstable owing to random fluctuations and differential diffusion. This gives rise to stationary wave patterns.

Excitable systems

Mechanochemical systems in which positive feedback and delayed negative feedback produce dynamical patterns of activity exhibiting bistability (a stable switch to an on or off state), pulses or oscillations. Spatial coupling mechanisms (for example, diffusion) lead to the emergence of waves of activity as illustrated in the classical example of the action potential.

Morphogenetic fields

Groups of cells responding to discrete, localized biochemical signals leading to the development of specific morphological structures or organs.

Mechanical stress

A physical quantity that expresses the mechanical forces that neighbouring particles of a continuous material exert on each other. It has the dimension of force per surface area (N m−2) or pressure (Pa).

Viscous response

Deformation of a viscous element, which resists shear flow and strain linearly with time when a stress is applied.

Boundary conditions

Constraints defining the limits of a system. In the case of morphogenesis these are typically the physical boundary of a tissue or an embryo.

Lateral line

A sensory system comprising clusters of mechanosensory epithelial cells (neuromasts) arranged as rosettes with their apical surface facing a shared lumen. The lateral line is initially established by a migratory group of cells, called a primordium, that deposits neuromasts at stereotyped locations along the surface of the fish.

Mena/VASP

Members of the VASP (vasodilator-stimulated phosphoprotein) family of proteins regulating the dynamics of the cortical actin cytoskeleton as downstream effectors of the Rho-family small G proteins Rac and Cdc42.

Shroom family proteins

Family of proteins characterized by a specific arrangement of an N-terminal PDZ domain, a central ASD1 (Apx/Shrm Domain 1) motif and a C-terminal ASD2 motif. ASD1 is required for targeting actin, while ASD2 is capable of eliciting an actomyosin constriction event.

Vitelline membrane

Structure surrounding the outer surface of blastoderm cells in embryos of several animals including birds and insects.

Convergence–extension

The process by which a tissue changes shape by narrowing (converging) in one direction and extending along a perpendicular axis.

Traction forces

Forces used to generate motion between a body and a tangential surface, through the use of friction or adhesion. Contractile systems anchored to a rigid body can generate traction forces to move cells or cellular objects.

Notochord

A small flexible rod made from cells from the mesoderm and oriented head to tail in embryos of organisms of the phylum Chordata. As it is composed of stiffer tissue, it allows for skeletal support of the embryo during development.

Germband

Blastoderm tissue corresponding to the ventrolateral region of the embryo in Drosophila melanogaster and other insects.

Primitive streak

Transient structure that forms in the blastula during the early stages of avian, reptilian and mammalian embryonic development. It forms on the dorsal (back) face of the embryo, towards the caudal or posterior end.

Marginal zone

Region corresponding to the equator between the two hemispheres in amphibian embryos.

Pair-rule genes

Group of genes expressed in stripes during segmentation of the embryo in arthropods. In Drosophila pair-rule genes form seven dorsoventrally oriented stripes disposed along the antero-posterior axis.

Toll receptors

A class of single-pass transmembrane receptors involved in patterning and immunity.

Parasegment

The fundamental unit of Drosophila melanogaster development, which is made up of portions of two adjacent segments along the body of the embryo.

Planar cell polarity

The coordinated polarization of a field of cells within the plane of a cell sheet. The axis of planar polarity is typically orthogonal to that of the apico-basal polarity of epithelial cells.

Septins

Cytoskeletal components that upon binding to GTP can polymerize into ordered structures such as rings and filaments, which can function as scaffolds or diffusion barriers.

Advection

The transport of a substance or physical quantity by the movement of the surrounding environment.

Dissipation timescale

Characteristic time at which the internal mechanical stress is reduced by a certain amount by viscous flow.

Bandpass filter

A filter or device that passes frequencies within a certain range and rejects frequencies outside that range.

Epiblast

Also known as primitive ectoderm. One of two distinct layers arising from the inner cell mass in the mammalian blastocyst or the blastodisc in avian and reptile embryos. In mammals, the epiblast sits between the trophectoderm and the hypoblast (or primitive endoderm).

Primitive endoderm

Also known as hypoblast. One of two layers arising from the inner cell mass in the mammalian blastocyst. The primitive endoderm sits between the epiblast and the blastocoel.

PVD neurons

Sensory neurons responding to harsh touch and cold temperatures with a highly elaborate dendritic arborization in the nematode Caenorhabditis elegans.

Vpda class I neurons

Sensory neurons of the peripheral nervous system of Drosophila melanogaster embryos and larvae. The classification is based on the morphology of the dendritic arborization with class I being the simplest morphology and class IV the most complex.

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Collinet, C., Lecuit, T. Programmed and self-organized flow of information during morphogenesis. Nat Rev Mol Cell Biol 22, 245–265 (2021). https://doi.org/10.1038/s41580-020-00318-6

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