Zebrafish airinemes optimize their shape between ballistic and diffusive search

  1. Sohyeon Park
  2. Hyunjoong Kim
  3. Yi Wang
  4. Dae Seok Eom  Is a corresponding author
  5. Jun Allard  Is a corresponding author
  1. University of California, Irvine, United States
  2. University of Pennsylvania, United States

Abstract

In addition to diffusive signals, cells in tissue also communicate via long, thin cellular protrusions, such as airinemes in zebrafish. Before establishing communication, cellular protrusions must find their target cell. Here we demonstrate that the shapes of airinemes in zebrafish are consistent with a finite persistent random walk model. The probability of contacting the target cell is maximized for a balance between ballistic search (straight) and diffusive search (highly curved, random). We find that the curvature of airinemes in zebrafish, extracted from live cell microscopy, is approximately the same value as the optimum in the simple persistent random walk model. We also explore the ability of the target cell to infer direction of the airineme's source, finding that there is a theoretical trade-off between search optimality and directional information. This provides a framework to characterize the shape, and performance objectives, of non-canonical cellular protrusions in general.

Data availability

Data and computational scripts are available in a repository mentioned in the manuscript (on GitHub)https://github.com/sohyeonparkgithub/Airineme-optimal-target-search

The following data sets were generated

Article and author information

Author details

  1. Sohyeon Park

    Center for Complex Biological Systems, University of California, Irvine, Irvine, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Hyunjoong Kim

    Department of Mathematics, University of Pennsylvania, Pennsylvania, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3534-2102
  3. Yi Wang

    Center for Complex Biological Systems, University of California, Irvine, Irvine, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7409-4335
  4. Dae Seok Eom

    Center for Complex Biological Systems, University of California, Irvine, Irvine, United States
    For correspondence
    dseom@uci.edu
    Competing interests
    The authors declare that no competing interests exist.
  5. Jun Allard

    dDepartment of Physics and Astronomy, University of California, Irvine, Irvine, United States
    For correspondence
    jun.allard@uci.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2758-4515

Funding

National Science Foundation (DMS-1454739)

  • Jun Allard

National Institutes of Health (R35GM142791)

  • Yi Wang
  • Dae Seok Eom

National Science Foundation (DMS 1763272)

  • Sohyeon Park
  • Jun Allard

Simons Foundation (594598,QN)

  • Sohyeon Park

Simons Foundation (Math+X U Penn)

  • Hyunjoong Kim

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

Ethics

Animal experimentation: All animal work in this study was conducted with the approval of the University of California Irvine Institutional Animal Care and Use Committee (Protocol #AUP-19-043) in accordance with institutional and federal guidelines for the ethical use of animals.

Reviewing Editor

  1. Pierre Sens, Institut Curie, CNRS UMR168, France

Version history

  1. Preprint posted: October 26, 2021 (view preprint)
  2. Received: November 19, 2021
  3. Accepted: April 25, 2022
  4. Accepted Manuscript published: April 25, 2022 (version 1)
  5. Version of Record published: May 12, 2022 (version 2)

Copyright

© 2022, Park 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. Sohyeon Park
  2. Hyunjoong Kim
  3. Yi Wang
  4. Dae Seok Eom
  5. Jun Allard
(2022)
Zebrafish airinemes optimize their shape between ballistic and diffusive search
eLife 11:e75690.
https://doi.org/10.7554/eLife.75690

Share this article

https://doi.org/10.7554/eLife.75690

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