The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors
Summary: Embryos develop in a concerted sequence of spatiotemporal arrangements of cells. In the preimplantation mouse embryo, the distribution of the cells in the inner cell mass evolves from a salt-and-pepper pattern to spatial segregation of two distinct cell types. The exact properties of the sa...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-11-01
|
| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223021831 |
| _version_ | 1797654691942760448 |
|---|---|
| author | Sabine C. Fischer Simon Schardt Joaquín Lilao-Garzón Silvia Muñoz-Descalzo |
| author_facet | Sabine C. Fischer Simon Schardt Joaquín Lilao-Garzón Silvia Muñoz-Descalzo |
| author_sort | Sabine C. Fischer |
| collection | DOAJ |
| description | Summary: Embryos develop in a concerted sequence of spatiotemporal arrangements of cells. In the preimplantation mouse embryo, the distribution of the cells in the inner cell mass evolves from a salt-and-pepper pattern to spatial segregation of two distinct cell types. The exact properties of the salt-and-pepper pattern have not been analyzed so far. We investigate the spatiotemporal distribution of NANOG- and GATA6-expressing cells in the ICM of the mouse blastocysts with quantitative three-dimensional single-cell-based neighborhood analyses. A combination of spatial statistics and agent-based modeling reveals that the cell fate distribution follows a local clustering pattern. Using ordinary differential equations modeling, we show that this pattern can be established by a distance-based signaling mechanism enabling cells to integrate information from the whole inner cell mass into their cell fate decision. Our work highlights the importance of longer-range signaling to ensure coordinated decisions in groups of cells to successfully build embryos. |
| first_indexed | 2024-03-11T17:03:12Z |
| format | Article |
| id | doaj.art-4e6d628a679d46d4b62e3ace3718c178 |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-11T17:03:12Z |
| publishDate | 2023-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-4e6d628a679d46d4b62e3ace3718c1782023-10-20T06:48:22ZengElsevieriScience2589-00422023-11-012611108106The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighborsSabine C. Fischer0Simon Schardt1Joaquín Lilao-Garzón2Silvia Muñoz-Descalzo3Julius-Maximilians-Universität Würzburg, Faculty of Biology, Center for Computational and Theoretical Biology, Klara-Oppenheimer-Weg 32, Campus Hubland Nord, 97074 Würzburg, Germany; Corresponding authorJulius-Maximilians-Universität Würzburg, Faculty of Biology, Center for Computational and Theoretical Biology, Klara-Oppenheimer-Weg 32, Campus Hubland Nord, 97074 Würzburg, GermanyInstituto Universitario de Investigaciones Biomédicas y Sanitarias (IUIBS), Universidad Las Palmas de Gran Canaria (ULPGC), Paseo Blas Cabrera Felipe ''Físico'' 17, Las Palmas de Gran Canaria 35016, SpainInstituto Universitario de Investigaciones Biomédicas y Sanitarias (IUIBS), Universidad Las Palmas de Gran Canaria (ULPGC), Paseo Blas Cabrera Felipe ''Físico'' 17, Las Palmas de Gran Canaria 35016, Spain; Corresponding authorSummary: Embryos develop in a concerted sequence of spatiotemporal arrangements of cells. In the preimplantation mouse embryo, the distribution of the cells in the inner cell mass evolves from a salt-and-pepper pattern to spatial segregation of two distinct cell types. The exact properties of the salt-and-pepper pattern have not been analyzed so far. We investigate the spatiotemporal distribution of NANOG- and GATA6-expressing cells in the ICM of the mouse blastocysts with quantitative three-dimensional single-cell-based neighborhood analyses. A combination of spatial statistics and agent-based modeling reveals that the cell fate distribution follows a local clustering pattern. Using ordinary differential equations modeling, we show that this pattern can be established by a distance-based signaling mechanism enabling cells to integrate information from the whole inner cell mass into their cell fate decision. Our work highlights the importance of longer-range signaling to ensure coordinated decisions in groups of cells to successfully build embryos.http://www.sciencedirect.com/science/article/pii/S2589004223021831Cellular physiologyDevelopmental biology |
| spellingShingle | Sabine C. Fischer Simon Schardt Joaquín Lilao-Garzón Silvia Muñoz-Descalzo The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors iScience Cellular physiology Developmental biology |
| title | The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| title_full | The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| title_fullStr | The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| title_full_unstemmed | The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| title_short | The salt-and-pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| title_sort | salt and pepper pattern in mouse blastocysts is compatible with signaling beyond the nearest neighbors |
| topic | Cellular physiology Developmental biology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223021831 |
| work_keys_str_mv | AT sabinecfischer thesaltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT simonschardt thesaltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT joaquinlilaogarzon thesaltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT silviamunozdescalzo thesaltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT sabinecfischer saltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT simonschardt saltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT joaquinlilaogarzon saltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors AT silviamunozdescalzo saltandpepperpatterninmouseblastocystsiscompatiblewithsignalingbeyondthenearestneighbors |