IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0233030.html
   My bibliography  Save this article

The transition from local to global patterns governs the differentiation of mouse blastocysts

Author

Listed:
  • Sabine C Fischer
  • Elena Corujo-Simon
  • Joaquin Lilao-Garzon
  • Ernst H K Stelzer
  • Silvia Muñoz-Descalzo

Abstract

During mammalian blastocyst development, inner cell mass (ICM) cells differentiate into epiblast (Epi) or primitive endoderm (PrE). These two fates are characterized by the expression of the transcription factors NANOG and GATA6, respectively. Here, we investigate the spatio-temporal distribution of NANOG and GATA6 expressing cells in the ICM of the mouse blastocysts with quantitative three-dimensional single cell-based neighbourhood analyses. We define the cell neighbourhood by local features, which include the expression levels of both fate markers expressed in each cell and its neighbours, and the number of neighbouring cells. We further include the position of a cell relative to the centre of the ICM as a global positional feature. Our analyses reveal a local three-dimensional pattern that is already present in early blastocysts: 1) Cells expressing the highest NANOG levels are surrounded by approximately nine neighbours, while 2) cells expressing GATA6 cluster according to their GATA6 levels. This local pattern evolves into a global pattern in the ICM that starts to emerge in mid blastocysts. We show that FGF/MAPK signalling is involved in the three-dimensional distribution of the cells and, using a mutant background, we further show that the GATA6 neighbourhood is regulated by NANOG. Our quantitative study suggests that the three-dimensional cell neighbourhood plays a role in Epi and PrE precursor specification. Our results highlight the importance of analysing the three-dimensional cell neighbourhood while investigating cell fate decisions during early mouse embryonic development.

Suggested Citation

  • Sabine C Fischer & Elena Corujo-Simon & Joaquin Lilao-Garzon & Ernst H K Stelzer & Silvia Muñoz-Descalzo, 2020. "The transition from local to global patterns governs the differentiation of mouse blastocysts," PLOS ONE, Public Library of Science, vol. 15(5), pages 1-29, May.
  • Handle: RePEc:plo:pone00:0233030
    DOI: 10.1371/journal.pone.0233030
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0233030
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0233030&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0233030?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sarah J. L. Graham & Krzysztof B. Wicher & Agnieszka Jedrusik & Guoji Guo & Wishva Herath & Paul Robson & Magdalena Zernicka-Goetz, 2014. "BMP signalling regulates the pre-implantation development of extra-embryonic cell lineages in the mouse embryo," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    2. Nicolas C. Rivron & Javier Frias-Aldeguer & Erik J. Vrij & Jean-Charles Boisset & Jeroen Korving & Judith Vivié & Roman K. Truckenmüller & Alexander Oudenaarden & Clemens A. Blitterswijk & Niels Geijs, 2018. "Blastocyst-like structures generated solely from stem cells," Nature, Nature, vol. 557(7703), pages 106-111, May.
    3. Yusuke Miyanari & Maria-Elena Torres-Padilla, 2012. "Control of ground-state pluripotency by allelic regulation of Nanog," Nature, Nature, vol. 483(7390), pages 470-473, March.
    4. Néstor Saiz & Kiah M. Williams & Venkatraman E. Seshan & Anna-Katerina Hadjantonakis, 2016. "Asynchronous fate decisions by single cells collectively ensure consistent lineage composition in the mouse blastocyst," Nature Communications, Nature, vol. 7(1), pages 1-14, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Nicolas Allègre & Sabine Chauveau & Cynthia Dennis & Yoan Renaud & Dimitri Meistermann & Lorena Valverde Estrella & Pierre Pouchin & Michel Cohen-Tannoudji & Laurent David & Claire Chazaud, 2022. "NANOG initiates epiblast fate through the coordination of pluripotency genes expression," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Nicolas Allègre & Sabine Chauveau & Cynthia Dennis & Yoan Renaud & Dimitri Meistermann & Lorena Valverde Estrella & Pierre Pouchin & Michel Cohen-Tannoudji & Laurent David & Claire Chazaud, 2022. "NANOG initiates epiblast fate through the coordination of pluripotency genes expression," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Mingyue Guo & Jinyi Wu & Chuanxin Chen & Xinggu Wang & An Gong & Wei Guan & Rowan M. Karvas & Kexin Wang & Mingwei Min & Yixuan Wang & Thorold W. Theunissen & Shaorong Gao & José C. R. Silva, 2024. "Self-renewing human naïve pluripotent stem cells dedifferentiate in 3D culture and form blastoids spontaneously," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Xinyu Hu & Bob van Sluijs & Óscar García-Blay & Yury Stepanov & Koen Rietrae & Wilhelm T. S. Huck & Maike M. K. Hansen, 2024. "ARTseq-FISH reveals position-dependent differences in gene expression of micropatterned mESCs," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Gemma Noviello & Rutger A. F. Gjaltema & Edda G. Schulz, 2023. "CasTuner is a degron and CRISPR/Cas-based toolkit for analog tuning of endogenous gene expression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Joyce J. Thompson & Daniel J. Lee & Apratim Mitra & Sarah Frail & Ryan K. Dale & Pedro P. Rocha, 2022. "Extensive co-binding and rapid redistribution of NANOG and GATA6 during emergence of divergent lineages," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Bas Loo & Simone A. Den & Nuno Araújo-Gomes & Vincent Jong & Rebecca R. Snabel & Maik Schot & José M. Rivera-Arbeláez & Gert Jan C. Veenstra & Robert Passier & Tom Kamperman & Jeroen Leijten, 2023. "Mass production of lumenogenic human embryoid bodies and functional cardiospheres using in-air-generated microcapsules," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Anna Malkowska & Christopher Penfold & Sophie Bergmann & Thorsten E. Boroviak, 2022. "A hexa-species transcriptome atlas of mammalian embryogenesis delineates metabolic regulation across three different implantation modes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0233030. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.