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Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis

Precise spatial patterning of cell fate during morphogenesis requires accurate inference of cellular position. In making such inferences from morphogen profiles, cells must contend with inherent stochasticity in morphogen production, transport, sensing and signalling. Motivated by the multitude of s...

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Autores principales: Iyer, Krishnan S, Prabhakara, Chaitra, Mayor, Satyajit, Rao, Madan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9988261/
https://www.ncbi.nlm.nih.gov/pubmed/36877545
http://dx.doi.org/10.7554/eLife.79257
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author Iyer, Krishnan S
Prabhakara, Chaitra
Mayor, Satyajit
Rao, Madan
author_facet Iyer, Krishnan S
Prabhakara, Chaitra
Mayor, Satyajit
Rao, Madan
author_sort Iyer, Krishnan S
collection PubMed
description Precise spatial patterning of cell fate during morphogenesis requires accurate inference of cellular position. In making such inferences from morphogen profiles, cells must contend with inherent stochasticity in morphogen production, transport, sensing and signalling. Motivated by the multitude of signalling mechanisms in various developmental contexts, we show how cells may utilise multiple tiers of processing (compartmentalisation) and parallel branches (multiple receptor types), together with feedback control, to bring about fidelity in morphogenetic decoding of their positions within a developing tissue. By simultaneously deploying specific and nonspecific receptors, cells achieve a more accurate and robust inference. We explore these ideas in the patterning of Drosophila melanogaster wing imaginal disc by Wingless morphogen signalling, where multiple endocytic pathways participate in decoding the morphogen gradient. The geometry of the inference landscape in the high dimensional space of parameters provides a measure for robustness and delineates stiff and sloppy directions. This distributed information processing at the scale of the cell highlights how local cell autonomous control facilitates global tissue scale design.
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spelling pubmed-99882612023-03-07 Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis Iyer, Krishnan S Prabhakara, Chaitra Mayor, Satyajit Rao, Madan eLife Developmental Biology Precise spatial patterning of cell fate during morphogenesis requires accurate inference of cellular position. In making such inferences from morphogen profiles, cells must contend with inherent stochasticity in morphogen production, transport, sensing and signalling. Motivated by the multitude of signalling mechanisms in various developmental contexts, we show how cells may utilise multiple tiers of processing (compartmentalisation) and parallel branches (multiple receptor types), together with feedback control, to bring about fidelity in morphogenetic decoding of their positions within a developing tissue. By simultaneously deploying specific and nonspecific receptors, cells achieve a more accurate and robust inference. We explore these ideas in the patterning of Drosophila melanogaster wing imaginal disc by Wingless morphogen signalling, where multiple endocytic pathways participate in decoding the morphogen gradient. The geometry of the inference landscape in the high dimensional space of parameters provides a measure for robustness and delineates stiff and sloppy directions. This distributed information processing at the scale of the cell highlights how local cell autonomous control facilitates global tissue scale design. eLife Sciences Publications, Ltd 2023-03-06 /pmc/articles/PMC9988261/ /pubmed/36877545 http://dx.doi.org/10.7554/eLife.79257 Text en © 2023, Iyer et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Iyer, Krishnan S
Prabhakara, Chaitra
Mayor, Satyajit
Rao, Madan
Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title_full Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title_fullStr Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title_full_unstemmed Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title_short Cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
title_sort cellular compartmentalisation and receptor promiscuity as a strategy for accurate and robust inference of position during morphogenesis
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9988261/
https://www.ncbi.nlm.nih.gov/pubmed/36877545
http://dx.doi.org/10.7554/eLife.79257
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