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Spontaneous phase coordination and fluid pumping in model ciliary carpets
Ciliated tissues, such as in the mammalian lungs, brains, and reproductive tracts, are specialized to pump fluid. They generate flows by the collective activity of hundreds of thousands of individual cilia that beat in a striking metachronal wave pattern. Despite progress in analyzing cilia coordina...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9659382/ https://www.ncbi.nlm.nih.gov/pubmed/36322751 http://dx.doi.org/10.1073/pnas.2214413119 |
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author | Kanale, Anup V. Ling, Feng Guo, Hanliang Fürthauer, Sebastian Kanso, Eva |
author_facet | Kanale, Anup V. Ling, Feng Guo, Hanliang Fürthauer, Sebastian Kanso, Eva |
author_sort | Kanale, Anup V. |
collection | PubMed |
description | Ciliated tissues, such as in the mammalian lungs, brains, and reproductive tracts, are specialized to pump fluid. They generate flows by the collective activity of hundreds of thousands of individual cilia that beat in a striking metachronal wave pattern. Despite progress in analyzing cilia coordination, a general theory that links coordination and fluid pumping in the limit of large arrays of cilia remains lacking. Here, we conduct in silico experiments with thousands of hydrodynamically interacting cilia, and we develop a continuum theory in the limit of infinitely many independently beating cilia by combining tools from active matter and classical Stokes flow. We find, in both simulations and theory, that isotropic and synchronized ciliary states are unstable. Traveling waves emerge regardless of initial conditions, but the characteristics of the wave and net flows depend on cilia and tissue properties. That is, metachronal phase coordination is a stable global attractor in large ciliary carpets, even under finite perturbations to cilia and tissue properties. These results support the notion that functional specificity of ciliated tissues is interlaced with the tissue architecture and cilia beat kinematics and open up the prospect of establishing structure to function maps from cilium-level beat to tissue-level coordination and fluid pumping. |
format | Online Article Text |
id | pubmed-9659382 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-96593822023-05-02 Spontaneous phase coordination and fluid pumping in model ciliary carpets Kanale, Anup V. Ling, Feng Guo, Hanliang Fürthauer, Sebastian Kanso, Eva Proc Natl Acad Sci U S A Biological Sciences Ciliated tissues, such as in the mammalian lungs, brains, and reproductive tracts, are specialized to pump fluid. They generate flows by the collective activity of hundreds of thousands of individual cilia that beat in a striking metachronal wave pattern. Despite progress in analyzing cilia coordination, a general theory that links coordination and fluid pumping in the limit of large arrays of cilia remains lacking. Here, we conduct in silico experiments with thousands of hydrodynamically interacting cilia, and we develop a continuum theory in the limit of infinitely many independently beating cilia by combining tools from active matter and classical Stokes flow. We find, in both simulations and theory, that isotropic and synchronized ciliary states are unstable. Traveling waves emerge regardless of initial conditions, but the characteristics of the wave and net flows depend on cilia and tissue properties. That is, metachronal phase coordination is a stable global attractor in large ciliary carpets, even under finite perturbations to cilia and tissue properties. These results support the notion that functional specificity of ciliated tissues is interlaced with the tissue architecture and cilia beat kinematics and open up the prospect of establishing structure to function maps from cilium-level beat to tissue-level coordination and fluid pumping. National Academy of Sciences 2022-11-02 2022-11-08 /pmc/articles/PMC9659382/ /pubmed/36322751 http://dx.doi.org/10.1073/pnas.2214413119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Kanale, Anup V. Ling, Feng Guo, Hanliang Fürthauer, Sebastian Kanso, Eva Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title | Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title_full | Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title_fullStr | Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title_full_unstemmed | Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title_short | Spontaneous phase coordination and fluid pumping in model ciliary carpets |
title_sort | spontaneous phase coordination and fluid pumping in model ciliary carpets |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9659382/ https://www.ncbi.nlm.nih.gov/pubmed/36322751 http://dx.doi.org/10.1073/pnas.2214413119 |
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