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

Wang, Zitong Jerry and Thomson, Matt (2022) Localization of signaling receptors maximizes cellular information acquisition in spatially structured natural environments. Cell Systems, 13 (7). pp. 530-546. ISSN 2405-4712. doi:10.1016/j.cels.2022.05.004. https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727

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Abstract

Cells in natural environments, such as 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 previously observed in cells maximizes information acquisition in simulated natural contexts, including tissue and soil. Specifically, information acquisition is maximized when receptors form localized patches at regions of maximal ligand concentration. 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cels.2022.05.004DOIArticle
https://doi.org/10.1101/2021.07.01.450787DOIDiscussion Paper
https://doi.org/10.5281/zenodo.6432083DOIData
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:© 2022 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 5 November 2021, Revised 8 February 2022, Accepted 12 May 2022, Available online 8 June 2022. We thank Michael Elowitz, Erik Winfree, and David Sivak for scientific discussions; 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. Author contributions: Conceptualization, Z.J.W. and M.T.; methodology, Z.J.W. and M.T.; manuscript writing, Z.J.W. and M.T.; supervision, M.T.; funding acquisition, M.T. Declaration of interests: M.T. is a member of the advisory board of Cell Systems. Data and code availability: All data have been deposited on the Caltech Research Data Repository and are publicly available as of the date of publication. DOIs are listed in the key resources table. All original code has been deposited at Zenodo (10.5281/zenodo.6432083) and is publicly available as of the date of publication. DOIs are listed in the key resources table. Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.
Group:Heritage Medical Research Institute
Funders:
Funding AgencyGrant Number
Heritage Medical Research InstituteUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
Subject Keywords:spatial organization; environmental statistics; cell migration; information theory; cell sensing; tissue microenvironment; synthetic circuit; haptotaxis; chemotaxis; search strategies
Issue or Number:7
DOI:10.1016/j.cels.2022.05.004
Record Number:CaltechAUTHORS:20210707-155629727
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727
Official Citation:Zitong Jerry Wang, Matt Thomson, Localization of signaling receptors maximizes cellular information acquisition in spatially structured natural environments, Cell Systems, Volume 13, Issue 7, 2022, Pages 530-546.e12, ISSN 2405-4712, https://doi.org/10.1016/j.cels.2022.05.004.
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:02 Aug 2022 17:42

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