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IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos
Architectural changes at the cellular and organism level are integral and necessary to successful development and growth. During mammalian preimplantation development, cells reduce in size and the architecture of the embryo changes significantly. Such changes must be coordinated correctly to ensure...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8341705/ https://www.ncbi.nlm.nih.gov/pubmed/34310594 http://dx.doi.org/10.1371/journal.pbio.3001345 |
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author | Forsyth, Jessica E. Al-Anbaki, Ali H. de la Fuente, Roberto Modare, Nikkinder Perez-Cortes, Diego Rivera, Isabel Seaton Kelly, Rowena Cotter, Simon Plusa, Berenika |
author_facet | Forsyth, Jessica E. Al-Anbaki, Ali H. de la Fuente, Roberto Modare, Nikkinder Perez-Cortes, Diego Rivera, Isabel Seaton Kelly, Rowena Cotter, Simon Plusa, Berenika |
author_sort | Forsyth, Jessica E. |
collection | PubMed |
description | Architectural changes at the cellular and organism level are integral and necessary to successful development and growth. During mammalian preimplantation development, cells reduce in size and the architecture of the embryo changes significantly. Such changes must be coordinated correctly to ensure continued development of the embryo and, ultimately, a successful pregnancy. However, the nature of such transformations is poorly defined during mammalian preimplantation development. In order to quantitatively describe changes in cell environment and organism architecture, we designed Internal Versus External Neighbourhood (IVEN). IVEN is a user-interactive, open-source pipeline that classifies cells into different populations based on their position and quantifies the number of neighbours of every cell within a dataset in a 3D environment. Through IVEN-driven analyses, we show how transformations in cell environment, defined here as changes in cell neighbourhood, are related to changes in embryo geometry and major developmental events during preimplantation mammalian development. Moreover, we demonstrate that modulation of the FGF pathway alters spatial relations of inner cells and neighbourhood distributions, leading to overall changes in embryo architecture. In conjunction with IVEN-driven analyses, we uncover differences in the dynamic of cell size changes over the preimplantation period and determine that cells within the mammalian embryo initiate growth phase only at the time of implantation. |
format | Online Article Text |
id | pubmed-8341705 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-83417052021-08-06 IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos Forsyth, Jessica E. Al-Anbaki, Ali H. de la Fuente, Roberto Modare, Nikkinder Perez-Cortes, Diego Rivera, Isabel Seaton Kelly, Rowena Cotter, Simon Plusa, Berenika PLoS Biol Methods and Resources Architectural changes at the cellular and organism level are integral and necessary to successful development and growth. During mammalian preimplantation development, cells reduce in size and the architecture of the embryo changes significantly. Such changes must be coordinated correctly to ensure continued development of the embryo and, ultimately, a successful pregnancy. However, the nature of such transformations is poorly defined during mammalian preimplantation development. In order to quantitatively describe changes in cell environment and organism architecture, we designed Internal Versus External Neighbourhood (IVEN). IVEN is a user-interactive, open-source pipeline that classifies cells into different populations based on their position and quantifies the number of neighbours of every cell within a dataset in a 3D environment. Through IVEN-driven analyses, we show how transformations in cell environment, defined here as changes in cell neighbourhood, are related to changes in embryo geometry and major developmental events during preimplantation mammalian development. Moreover, we demonstrate that modulation of the FGF pathway alters spatial relations of inner cells and neighbourhood distributions, leading to overall changes in embryo architecture. In conjunction with IVEN-driven analyses, we uncover differences in the dynamic of cell size changes over the preimplantation period and determine that cells within the mammalian embryo initiate growth phase only at the time of implantation. Public Library of Science 2021-07-26 /pmc/articles/PMC8341705/ /pubmed/34310594 http://dx.doi.org/10.1371/journal.pbio.3001345 Text en © 2021 Forsyth et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Methods and Resources Forsyth, Jessica E. Al-Anbaki, Ali H. de la Fuente, Roberto Modare, Nikkinder Perez-Cortes, Diego Rivera, Isabel Seaton Kelly, Rowena Cotter, Simon Plusa, Berenika IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title | IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title_full | IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title_fullStr | IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title_full_unstemmed | IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title_short | IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos |
title_sort | iven: a quantitative tool to describe 3d cell position and neighbourhood reveals architectural changes in fgf4-treated preimplantation embryos |
topic | Methods and Resources |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8341705/ https://www.ncbi.nlm.nih.gov/pubmed/34310594 http://dx.doi.org/10.1371/journal.pbio.3001345 |
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