scholarly journals A critical-like collective state leads to long-range cell communication in Dictyostelium discoideum aggregation

PLoS Biology ◽  
2017 ◽  
Vol 15 (4) ◽  
pp. e1002602 ◽  
Author(s):  
Giovanna De Palo ◽  
Darvin Yi ◽  
Robert G. Endres
2016 ◽  
Author(s):  
Giovanna De Palo ◽  
Darvin Yi ◽  
Robert G. Endres

AbstractThe transition from single-cell to multicellular behavior is important in early development but rarely studied. The starvation-induced aggregation of the social amoeba Dictyostelium discoideum into a multicellular slug is known to result from single-cell chemotaxis towards emitted pulses of cyclic adenosine monophosphate (cAMP). However, how exactly do transient short-range chemical gradients lead to coherent collective movement at a macroscopic scale? Here, we developed a multiscale model verified by quantitative microscopy to describe wide-ranging behaviors from chemotaxis and excitability of individual cells to aggregation of thousands of cells. To better understand the mechanism of long-range cell-cell communication and hence aggregation, we analyzed cell-cell correlations, showing evidence of self-organization at the onset of aggregation (as opposed to following a leader cell). Surprisingly, cell collectives, despite their finite size, show features of criticality known from phase transitions in physical systems. By comparing wild-type and mutant cells with impaired aggregation, we found the longest cellcell communication distance in wild-type cells, suggesting that criticality provides an adaptive advantage and optimally sized aggregates for the dispersal of spores.Author SummaryCells are often coupled to each other in cell collectives, such as aggregates during early development, tissues in the developed organism, and tumors in disease. How do cells communicate over macroscopic distances much larger than the typical cell-cell distance to decide how they should behave? Here, we developed a multiscale model of social amoeba, spanning behavior from individuals to thousands of cells. We show that local cell-cell coupling via secreted chemicals may be tuned to a critical value, resulting in emergent long-range communication and heightened sensitivity. Hence, these aggregates are remarkably similar to bacterial biofilms and neuronal networks, all communicating in a pulse-like fashion. Similar organizing principles may also aid our understanding of the remarkable robustness in cancer development.


2020 ◽  
Author(s):  
Assaf Nahum ◽  
Yoni Koren ◽  
Sari Natan ◽  
Shahar Goren ◽  
Ayelet Lesman ◽  
...  

AbstractCells sense, manipulate and respond to the mechanical properties of their microenvironment in a plethora of physiological processes, yet whether and how cells interpret environmental cues to communicate with distant cells is mostly unknown. We present a computational method to systematically infer and quantify long-range mechanical cell-cell communication through the extracellular matrix (cell-ECM-cell communication). By correlating local ECM remodeling fluctuations, in finite element simulations and live 3D imaging of fibroblasts embedded in fibrin gels, our method matched pairs of communicating cells with high accuracy, and identified whether and to what extent one cell was influenced by its communication partner. Using this method, we revealed that cells actively respond to the mechanical signal that they sense from the other cell, amplifying the formation of a dense fibrin band between the communicating cells. Our method sets the stage to measure the fundamental aspects of intercellular long-range mechanical communication in physiological contextes and may provide a new functional readout for high content 3D image-based screening.


2020 ◽  
Author(s):  
O. Cochet-Escartin ◽  
M. Demircigil ◽  
S. Hirose ◽  
B. Allais ◽  
P. Gonzalo ◽  
...  

AbstractIt is well known that eukaryotic cells can sense oxygen (O2) and adapt their metabolism accordingly. It is less known that they can also move towards regions of higher oxygen level (aerotaxis). Using a self-generated hypoxic assay, we show that the social amoeba Dictyostelium discoideum displays a spectacular aerotactic behavior. When a cell colony is covered by a coverglass, cells quickly consume the available O2 and the ones close to the periphery move directionally outward forming a dense ring keeping a constant speed and density. To confirm that O2 is the main molecular player in this seemingly collective process, we combined two technological developments, porphyrin based O2 sensing films and microfluidic O2 gradient generators. We showed that Dictyostelium cells exhibit aerotactic and aerokinetic (increased speed at low O2) response in an extremely low range of O2 concentration (0-1.5%) indicative of a very efficient detection mechanism. The various cell behaviors under self-generated or imposed O2 gradients were modeled with a very satisfactory quantitative agreement using an in silico cellular Potts model built on experimental observations. This computational model was complemented with a parsimonious ‘Go or Grow’ partial differential equation (PDE) model. In both models, we found that the collective migration of a dense ring can be explained by the interplay between cell division and the modulation of aerotaxis, without the need for cell-cell communication.


2014 ◽  
Vol 5 (1) ◽  
Author(s):  
Akihiko Nakajima ◽  
Shuji Ishihara ◽  
Daisuke Imoto ◽  
Satoshi Sawai

2019 ◽  
Vol 12 (2) ◽  
pp. 258-273 ◽  
Author(s):  
Jara Obermann ◽  
Felicia Wagner ◽  
Anita Kociaj ◽  
Alessandro Zambusi ◽  
Jovica Ninkovic ◽  
...  

Sign in / Sign up

Export Citation Format

Share Document