Cells use molecular working memory to navigate inchanging chemoattractant fields

  1. Akhilesh Nandan
  2. Abhishek Das
  3. Robert Lott
  4. Aneta Koseska  Is a corresponding author
  1. Max Planck Institute for Neurobiology of Behavior - caesar, Germany
  2. Max Planck Institute of Molecular Physiology, Germany

Abstract

In order to migrate over large distances, cells within tissues and organisms rely on sensing local gradient cues which are irregular, conflicting, and changing over time and space. The mechanism how they generate persistent directional migration when signals are disrupted, while still remaining adaptive to signal's localization changes remain unknown. Here we find that single cells utilize a molecular mechanism akin to a working memory to satisfy these two opposing demands. We derive theoretically that this is characteristic for receptor networks maintained away from steady states. Time-resolved live-cell imaging of Epidermal growth factor receptor (EGFR) phosphorylation dynamics shows that cells transiently memorize position of encountered signals via slow-escaping remnant of the polarized signaling state, a dynamical 'ghost', driving memory-guided persistent directional migration. The metastability of this state further enables migrational adaptation when encountering new signals. We thus identify basic mechanism of real-time computations underlying cellular navigation in changing chemoattractant fields.

Data availability

Source data is provided with the submission. The numerical data used to generate the corresponding figures can be obtained from the codes deposited in https://github.com/akhileshpnn/Cell-memory.

The following data sets were generated

Article and author information

Author details

  1. Akhilesh Nandan

    Cellular Computations and Learning, Max Planck Institute for Neurobiology of Behavior - caesar, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Abhishek Das

    Cellular Computations and Learning, Max Planck Institute for Neurobiology of Behavior - caesar, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert Lott

    Cellular Computations and Learning, Max Planck Institute for Neurobiology of Behavior - caesar, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Aneta Koseska

    Department of Systemic Cell Biology, Max Planck Institute of Molecular Physiology, Dortmund, Germany
    For correspondence
    aneta.koseska@mpinb.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4263-2340

Funding

Max Planck Society

  • Aneta Koseska

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

Reviewing Editor

  1. Arvind Murugan, University of Chicago, United States

Version history

  1. Preprint posted: November 12, 2021 (view preprint)
  2. Received: January 6, 2022
  3. Accepted: June 3, 2022
  4. Accepted Manuscript published: June 6, 2022 (version 1)
  5. Version of Record published: July 14, 2022 (version 2)

Copyright

© 2022, Nandan 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. Akhilesh Nandan
  2. Abhishek Das
  3. Robert Lott
  4. Aneta Koseska
(2022)
Cells use molecular working memory to navigate inchanging chemoattractant fields
eLife 11:e76825.
https://doi.org/10.7554/eLife.76825

Share this article

https://doi.org/10.7554/eLife.76825

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