Molecular-Level Tuning of Cellular Autonomy Controls the Collective Behaviors of Cell Populations

Théo Maire; Hyun Youk

doi:10.1016/j.cels.2015.10.012

Molecular-Level Tuning of Cellular Autonomy Controls the Collective Behaviors of Cell Populations

Cell Syst. 2015 Nov 25;1(5):349-60. doi: 10.1016/j.cels.2015.10.012. Epub 2015 Nov 25.

Authors

Théo Maire¹, Hyun Youk²

Affiliations

¹ Department of Biology, École Normale Supérieure, Paris 75005, France; Department of Bionanoscience, Delft University of Technology, Delft 2628, the Netherlands; Kavli Institute of Nanoscience, Delft University of Technology, Delft 2628, the Netherlands.
² Department of Bionanoscience, Delft University of Technology, Delft 2628, the Netherlands; Kavli Institute of Nanoscience, Delft University of Technology, Delft 2628, the Netherlands. Electronic address: h.youk@tudelft.nl.

PMID: 27136241
DOI: 10.1016/j.cels.2015.10.012

Abstract

A rigorous understanding of how multicellular behaviors arise from the actions of single cells requires quantitative frameworks that bridge the gap between genetic circuits, the arrangement of cells in space, and population-level behaviors. Here, we provide such a framework for a ubiquitous class of multicellular systems-namely, "secrete-and-sense cells" that communicate by secreting and sensing a signaling molecule. By using formal, mathematical arguments and introducing the concept of a phenotype diagram, we show how these cells tune their degrees of autonomous and collective behavior to realize distinct single-cell and population-level phenotypes; these phenomena have biological analogs, such as quorum sensing or paracrine signaling. We also define the "entropy of population," a measurement of the number of arrangements that a population of cells can assume, and demonstrate how a decrease in the entropy of population accompanies the formation of ordered spatial patterns. Our conceptual framework ties together diverse systems, including tissues and microbes, with common principles.