Cargando…

Migration and division in cell monolayers on substrates with topological defects

Collective movement and organization of cell monolayers are important for wound healing and tissue development. Recent experiments highlighted the importance of liquid crystal order within these layers, suggesting that +1 topological defects have a role in organizing tissue morphogenesis. We study f...

Descripción completa

Detalles Bibliográficos
Autores principales: Kaiyrbekov, Kurmanbek, Endresen, Kirsten, Sullivan, Kyle, Zheng, Zhaofei, Chen, Yun, Serra, Francesca, Camley, Brian A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372565/
https://www.ncbi.nlm.nih.gov/pubmed/37463218
http://dx.doi.org/10.1073/pnas.2301197120
_version_ 1785078397906452480
author Kaiyrbekov, Kurmanbek
Endresen, Kirsten
Sullivan, Kyle
Zheng, Zhaofei
Chen, Yun
Serra, Francesca
Camley, Brian A.
author_facet Kaiyrbekov, Kurmanbek
Endresen, Kirsten
Sullivan, Kyle
Zheng, Zhaofei
Chen, Yun
Serra, Francesca
Camley, Brian A.
author_sort Kaiyrbekov, Kurmanbek
collection PubMed
description Collective movement and organization of cell monolayers are important for wound healing and tissue development. Recent experiments highlighted the importance of liquid crystal order within these layers, suggesting that +1 topological defects have a role in organizing tissue morphogenesis. We study fibroblast organization, motion, and proliferation on a substrate with micron-sized ridges that induce +1 and −1 topological defects using simulation and experiment. We model cells as self-propelled deformable ellipses that interact via a Gay–Berne potential. Unlike earlier work on other cell types, we see that density variation near defects is not explained by collective migration. We propose instead that fibroblasts have different division rates depending on their area and aspect ratio. This model captures key features of our previous experiments: the alignment quality worsens at high cell density and, at the center of the +1 defects, cells can adopt either highly anisotropic or primarily isotropic morphologies. Experiments performed with different ridge heights confirm a prediction of this model: Suppressing migration across ridges promotes higher cell density at the +1 defect. Our work enables a mechanism for tissue patterning using topological defects without relying on cell migration.
format Online
Article
Text
id pubmed-10372565
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-103725652023-07-28 Migration and division in cell monolayers on substrates with topological defects Kaiyrbekov, Kurmanbek Endresen, Kirsten Sullivan, Kyle Zheng, Zhaofei Chen, Yun Serra, Francesca Camley, Brian A. Proc Natl Acad Sci U S A Physical Sciences Collective movement and organization of cell monolayers are important for wound healing and tissue development. Recent experiments highlighted the importance of liquid crystal order within these layers, suggesting that +1 topological defects have a role in organizing tissue morphogenesis. We study fibroblast organization, motion, and proliferation on a substrate with micron-sized ridges that induce +1 and −1 topological defects using simulation and experiment. We model cells as self-propelled deformable ellipses that interact via a Gay–Berne potential. Unlike earlier work on other cell types, we see that density variation near defects is not explained by collective migration. We propose instead that fibroblasts have different division rates depending on their area and aspect ratio. This model captures key features of our previous experiments: the alignment quality worsens at high cell density and, at the center of the +1 defects, cells can adopt either highly anisotropic or primarily isotropic morphologies. Experiments performed with different ridge heights confirm a prediction of this model: Suppressing migration across ridges promotes higher cell density at the +1 defect. Our work enables a mechanism for tissue patterning using topological defects without relying on cell migration. National Academy of Sciences 2023-07-18 2023-07-25 /pmc/articles/PMC10372565/ /pubmed/37463218 http://dx.doi.org/10.1073/pnas.2301197120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Physical Sciences
Kaiyrbekov, Kurmanbek
Endresen, Kirsten
Sullivan, Kyle
Zheng, Zhaofei
Chen, Yun
Serra, Francesca
Camley, Brian A.
Migration and division in cell monolayers on substrates with topological defects
title Migration and division in cell monolayers on substrates with topological defects
title_full Migration and division in cell monolayers on substrates with topological defects
title_fullStr Migration and division in cell monolayers on substrates with topological defects
title_full_unstemmed Migration and division in cell monolayers on substrates with topological defects
title_short Migration and division in cell monolayers on substrates with topological defects
title_sort migration and division in cell monolayers on substrates with topological defects
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10372565/
https://www.ncbi.nlm.nih.gov/pubmed/37463218
http://dx.doi.org/10.1073/pnas.2301197120
work_keys_str_mv AT kaiyrbekovkurmanbek migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT endresenkirsten migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT sullivankyle migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT zhengzhaofei migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT chenyun migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT serrafrancesca migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects
AT camleybriana migrationanddivisionincellmonolayersonsubstrateswithtopologicaldefects