Dynamics of diffusive cell signaling relays

  1. Paul B Dieterle
  2. Jiseon Min
  3. Daniel Irimia
  4. Ariel Amir  Is a corresponding author
  1. Harvard University, United States
  2. Massachusetts General Hopital, Harvard Medical School, United States

Abstract

In biological contexts as diverse as development, apoptosis, and synthetic microbial consortia, collections of cells or sub-cellular components have been shown to overcome the slow signaling speed of simple diffusion by utilizing diffusive relays, in which the presence of one type of diffusible signaling molecule triggers participation in the emission of the same type of molecule. This collective effect gives rise to fast-traveling diffusive waves. Here, in the context of cell signaling, we show that system dimensionality – the shape of the extracellular medium and the distribution of cells within it – can dramatically affect the wave dynamics, but that these dynamics are insensitive to details of cellular activation. As an example, we show that neutrophil swarming experiments exhibit dynamical signatures consistent with the proposed signaling motif. We further show that cell signaling relays generate much steeper concentration profiles than does simple diffusion, which may facilitate neutrophil chemotaxis.

Data availability

The only dataset we analyze or generate is present and available in Reategui (2017). PMID: 29057147. Code for the figures is available at github.io/pdieterle/diffWavePropAndInit.

The following previously published data sets were used

Article and author information

Author details

  1. Paul B Dieterle

    Physics, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jiseon Min

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel Irimia

    Surgery, Massachusetts General Hopital, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7347-2082
  4. Ariel Amir

    Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, United States
    For correspondence
    arielamir@seas.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2611-0139

Funding

National Science Foundation (MRSEC DMR 14-20570)

  • Ariel Amir

Kavli Foundation (N/A)

  • Ariel Amir

National Science Foundation (CAREER 1752024)

  • Ariel Amir

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Received: August 4, 2020
  2. Accepted: December 3, 2020
  3. Accepted Manuscript published: December 4, 2020 (version 1)
  4. Version of Record published: January 4, 2021 (version 2)

Copyright

© 2020, Dieterle et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Paul B Dieterle
  2. Jiseon Min
  3. Daniel Irimia
  4. Ariel Amir
(2020)
Dynamics of diffusive cell signaling relays
eLife 9:e61771.
https://doi.org/10.7554/eLife.61771

Share this article

https://doi.org/10.7554/eLife.61771

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