Do embryonic cells communicate via mechanical feedback?

By Tom Sharp on August 30, 2016

The survival of multicellular organisms relies on the harmonization of cellular activities, which can only be achieved with a high level of intercellular communication. In a recent Special Issue on 50 years of liquid state theory, Professor Jerzy Blawzdziewicz and his team provide compelling evidence that mechanical feedback helps coordinate individual cellular activity during embryonic development. Read on to find out more from the authors themselves.

When one thinks of cellular communication, chemical signaling is often the first—if not the only—form of communication that comes to mind. The importance of chemical signaling between cells is indisputable; however, there is mounting evidence that a substantial portion of intercellular communication, especially during embryonic development, may actually occur through mechanical signaling (via intercellular forces) in many diverse biological phenomena. For example, the Liu Research Group from the University of Pennsylvania recently reported at the APS March 2016 Meeting that embryonic heartbeats are coordinated mechanically rather than electrically, contrary to what happens in the adult heart.

Figure: Underside image of a wild-type common fruit fly embryo (top) and active granular fluid model (bottom) with constricted cells/particles shown in brown. The strong similarity between the patterns formed reveals that cellular constrictions may rely on cellular communication through mechanical feedback. © 2016 IOP Publishing Ltd. All rights reserved.

The motivation behind our current research is to understand cellular mechanical coordination and find ways to quantitatively analyze intercellular mechanical interactions. In our recently published JPCM article, we present a mechanically sensitive Active Granular Fluid model of the bottom (ventral) side of a common fruit fly embryo. Cells of the embryo are represented as interconnected circular particles that undergo random constrictions but are more likely to constrict depending on the stress they experience from their neighboring particles. Our model revealed that particles which are sensitive to pulling (tensile) stress tend to form strongly correlated chain-like structures that are remarkably similar to patterns (cellular constriction chains) observed in vivo (as shown in the figure). This strong agreement provides compelling evidence that mechanical feedback plays an important role during the early stages of embryonic development. In our paper we provide an analysis and a map of this process.

Our Active Granular Fluid model may provide a promising means of analyzing tissues. We believe that active granular fluid modeling can be used to quantitatively analyze local intercellular mechanical interactions and tissue-wide mechanical stress fields. In our future work we will develop our model into a tool for quantitative analysis of the whole embryo. We also plan to expand this modeling platform to investigate other complex biological processes. Although we have thus far focused our efforts on modeling the common fruit fly embryo, we expect that our model will be useful to study other organisms commonly used by biologists in fundamental research such as C. elegans (a tiny, one-millimeter long transparent worm) and Zebrafish.

In addition to the work discussed here, other students in our group are involved in the development of models describing C. elegans locomotion and maneuverability, and chemotaxis in both two- and three-dimensional complex environments. The intermeshing of physics and biology is an expanding frontier in science. The granular physics community, and more generally the condensed matter community, has much to offer towards the elucidation of biological phenomena.

Guo-Jie Jason Gao was an assistant professor in the Department of Mechanical Engineering at National Taiwan University. He recently joined the Department of Mathematical and Systems Engineering at Shizuoka University in Japan. He works on understanding the non-equilibrium behavior of glassy, granular, and nanostructured materials.

Michael C. Holcomb is a doctoral candidate of the Texas Tech University Department of Physics. His research in biophysics is primarily focused on the nonlinear and complex systems phenomena found in the developing Drosophila melanogaster embryo.

Jeffrey H. Thomas is a developmental biologist in the Department of Cell Biology and Biochemistry at Texas Tech University Health Sciences Center. His work focuses on the morphogenesis of cells and tissues in the developing Drosophila melanogaster embryo.

Jerzy Blawzdziewicz is a professor of mechanical engineering and physics at Texas Tech University. He investigates the microstructure and mechanical properties of soft matter and biological matter. He uses theoretical methods and numerical simulations to study microscale phenomena in complex fluids, nanomaterials, glassy materials, and granular matter; his research interests also include biomechanics of locomotion and tissue development.

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