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Signaling receptor localization maximizes cellular information acquisition in spatially-structured, natural environments

Wang, Zitong Jerry and Thomson, Matt (2021) Signaling receptor localization 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 (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727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 that are sculpted by processes such as fluid flow and substrate adhesion. Nevertheless, traditional approaches to studying cell sensing assume signals are either uniform or monotonic, neglecting spatial structures of natural environments. 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. By viewing cell surface receptors as a sensor network, we develop an information theoretic framework for computing the optimal spatial organization of a sensing system for a given spatial signaling environment. Applying the framework to simulated environments, we find that spatial receptor localization maximizes information acquisition in many natural contexts, including tissue and soil. Receptor localization extends naturally to produce a dynamic protocol for redistributing signaling receptors during cell navigation and can be implemented in a cell using a feedback scheme. In a simulated tissue environment, dynamic receptor localization boosts navigation efficiency by 30-fold. Broadly, our framework readily adapts to studying how the spatial organization of signaling components other than receptors can be modulated to improve cellular information processing.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.07.01.450787DOIDiscussion Paper
ORCID:
AuthorORCID
Wang, Zitong Jerry0000-0001-8008-7318
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. This version posted July 2, 2021. We thank Michael Elowitz and Erik Winfree for scientific discussions and Dominik Schildknecht, Tae Han Kim, Pranav Bhamidipati, Abdullah Farooq, for feedback on the manuscript. 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.
Group:Heritage Medical Research Institute
Funders:
Funding AgencyGrant Number
Heritage Medical Research InstituteUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
Record Number:CaltechAUTHORS:20210707-155629727
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210707-155629727
Official Citation:Signaling receptor localization 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:08 Jul 2021 17:16

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