Abstract
Biological systems display a rich phenomenology of states that resemble the physical states of matter - solid, liquid and gas. These phases result from the interactions between the microscopic constituent components - the cells - that manifest in macroscopic properties such as fluidity, rigidity and resistance to changes in shape and volume. Looked at from such a perspective, phase transitions from a rigid to a flowing state or vice versa define much of what happens in many biological processes especially during early development and diseases such as cancer. Additionally, collectively moving confluent cells can also lead to kinematic phase transitions in biological systems similar to multi-particle systems where the particles can interact and show sub-populations characterised by specific velocities. In this Perspective we discuss the similarities and limitations of the analogy between biological and inert physical systems both from theoretical perspective as well as experimental evidence in biological systems. In understanding such transitions, it is crucial to acknowledge that the macroscopic properties of biological materials and their modifications result from the complex interplay between the microscopic properties of cells including growth or death, neighbour interactions and secretion of matrix, phenomena unique to biological systems. Detecting phase transitions in vivo is technically difficult. We present emerging approaches that address this challenge and may guide our understanding of the organization and macroscopic behaviour of biological tissues.
Highlights
Biological systems display a rich phenomenology of such states of matter that result from the interaction of cells with their neighbors and the extracellular media, which is often created by the cells themselves (Fig. 1)
A true solid-like behavior, distinguished by resistance to shape and volume changes, is often displayed in scenarios when the cells are completely replaced by their own extracellular matrix (ECM) or mineral secretions over time (Fig. 1)
A collection of mesenchymal cells can still be confined within a small region despite large movements at the individual level and result in the overall structural stability of the region. Evidence of such a fluid-to-solid transition in mesenchyme was recently elucidated in the context of the gradual “solidification” of tissue in the zebrafish mesodermal progenitor zone as cells move into presomitic mesoderm, where they are more packed[2]
Summary
Biological systems display a rich phenomenology of states that resemble the physical states of matter - solid, liquid and gas These phases result from the interactions between the microscopic constituent components - the cells - that manifest in macroscopic properties such as fluidity, rigidity and resistance to changes in shape and volume. In cell monolayers undergoing a transition that resembles the jamming transition (Box 2), it was proposed to replace the temperature by cell motility, volume fraction by the density, and stress by the inverse of cell–cell adhesion (Fig. 2)[18] These parameters have molecular origins and can result in changes at the cellular and multicellular levels leading to phase transitions. In particular for zebrafish embryos, the first 2.5 h of development are accompanied by synchronous cell divisions almost every 15 min, effectively implying that all cells undergo mitotic cell rounding and loose cell–cell contact every 15 min
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