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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Main Authors: Jessica E Forsyth, Ali H Al-Anbaki, Roberto de la Fuente, Nikkinder Modare, Diego Perez-Cortes, Isabel Rivera, Rowena Seaton Kelly, Simon Cotter, Berenika Plusa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-07-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001345&type=printable
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author Jessica E Forsyth
Ali H Al-Anbaki
Roberto de la Fuente
Nikkinder Modare
Diego Perez-Cortes
Isabel Rivera
Rowena Seaton Kelly
Simon Cotter
Berenika Plusa
author_facet Jessica E Forsyth
Ali H Al-Anbaki
Roberto de la Fuente
Nikkinder Modare
Diego Perez-Cortes
Isabel Rivera
Rowena Seaton Kelly
Simon Cotter
Berenika Plusa
author_sort Jessica E Forsyth
collection DOAJ
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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institution Kabale University
issn 1544-9173
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spelling doaj-art-e0f5a5b746b64ad780975bfb580a57562025-08-20T03:44:40ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852021-07-01197e300134510.1371/journal.pbio.3001345IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos.Jessica E ForsythAli H Al-AnbakiRoberto de la FuenteNikkinder ModareDiego Perez-CortesIsabel RiveraRowena Seaton KellySimon CotterBerenika PlusaArchitectural 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001345&type=printable
spellingShingle Jessica E Forsyth
Ali H Al-Anbaki
Roberto de la Fuente
Nikkinder Modare
Diego Perez-Cortes
Isabel Rivera
Rowena Seaton Kelly
Simon Cotter
Berenika Plusa
IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos.
PLoS Biology
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
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001345&type=printable
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