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Localization of signaling receptors maximizes cellular information acquisition in spatially-structured natural environments

Wang, Zitong Jerry and Thomson, Matt (2021) Localization of signaling receptors maximizes cellular information acquisition in spatially-structured natural environments. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727

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Abstract

Cells in natural environments like tissue or soil sense and respond to extracellular ligands with intricately structured and non-monotonic spatial distributions, sculpted by processes such as fluid flow and substrate adhesion. In this work, we show that spatial sensing and navigation can be optimized by adapting the spatial organization of signaling pathways to the spatial structure of the environment. We develop an information-theoretic framework for computing the optimal spatial organization of a sensing system for a given signaling environment. We find that receptor localization maximizes information acquisition in simulated natural contexts, including tissue and soil. Receptor localization extends naturally to produce a dynamic protocol for continuously redistributing signaling receptors, which when implemented using simple feedback, boosts cell navigation efficiency by 30-fold. Broadly, our work shows how cells can maximize the fidelity of information transfer by adapting the spatial organization of signaling molecules to the spatial structure of the environment.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.07.01.450787DOIDiscussion Paper
https://github.com/neonine2/receptor-codeRelated ItemCode
http://dx.doi.org/10.22002/D1.2149DOIData
ORCID:
AuthorORCID
Wang, Zitong Jerry0000-0001-8008-7318
Thomson, Matt0000-0003-1021-1234
Alternate Title:Signaling receptor localization maximizes cellular information acquisition in spatially-structured, natural environments, Receptor localization maximizes information acquisition in natural cell environments
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Version 1 - July 2, 2021; Version 2 - October 19, 2021; Version 3 - November 8, 2021; Version 4 - February 15, 2022. We thank Michael Elowitz, Erik Winfree, and David Sivak for scientific discussions and Dominik Schildknecht, Han Kim, Guruprasad Raghavan, Pranav Bhamidipati, Abdullah Farooq, for feedback on the manuscript, Inna-Marie Strazhnik for illustrations, and Angela Anderson for editorial advice. We also would like to thank Eugenio Marco and Katarzyna Rejniak for technical advice with receptor feedback and tissue simulations, respectively. The authors would like to acknowledge the Heritage Medical Research Institute and Packard Foundation for funding and intellectual support. Data availability: All analysis, simulation and plotting scripts are openly available at: https://github.com/neonine2/receptor-code. All data generated in this work is openly available at: http://dx.doi.org/10.22002/D1.2149. Material availability: This paper did not generate new reagents. Author Contributions: Conceptualization, Z.W. and M.T.; Methodology, Z.W. and M.T.; Manuscript writing, Z.W. and M.T.; Supervision, M.T.; Funding acquisition, M.T. The authors declare no competing interests.
Group:Heritage Medical Research Institute
Funders:
Funding AgencyGrant Number
Heritage Medical Research InstituteUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
Subject Keywords:spatial organization, natural environmental statistics, cell navigation, information processing, cell sensing
DOI:10.1101/2021.07.01.450787
Record Number:CaltechAUTHORS:20210707-155629727
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727
Official Citation:Localization of signaling receptors maximizes cellular information acquisition in spatially-structured natural environments. Zitong Jerry Wang, Matt Thomson. bioRxiv 2021.07.01.450787; doi: https://doi.org/10.1101/2021.07.01.450787
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109742
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:08 Jul 2021 17:16
Last Modified:16 Feb 2022 18:04

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