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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2023
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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. |
format | Online Article Text |
id | pubmed-9988261 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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