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Pré-Publication, Document De Travail Année : 2020

Hypoxia triggers collective aerotactic migration in Dictyostelium discoideum

Résumé

It is well known that eukaryotic cells can sense oxygen (O 2 ) 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 O 2 and the ones close to the periphery move directionally outward forming a dense ring keeping a constant speed and density. To confirm that O 2 is the main molecular player in this seemingly collective process, we combined two technological developments, porphyrin based O 2 sensing films and microfluidic O 2 gradient generators. We showed that Dictyostelium cells exhibit aerotactic and aerokinetic (increased speed at low O 2 ) response in an extremely low range of O 2 concentration (0-1.5%) indicative of a very efficient detection mechanism. The various cell behaviors under self-generated or imposed O 2 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. Explicit wave solutions of the PDE model also informed about the relative contributions of division and directed motion on the collective speed.
It 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. Explicit wave solutions of the PDE model also informed about the relative contributions of division and directed motion on the collective speed.
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Dates et versions

hal-02997747 , version 1 (12-11-2020)
hal-02997747 , version 2 (02-09-2021)

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Olivier Cochet-Escartin, M. Demircigil, S. Hirose, B. Allais, V. Calvez, et al.. Hypoxia triggers collective aerotactic migration in Dictyostelium discoideum. 2020. ⟨hal-02997747v1⟩
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