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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
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.
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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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