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6. Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids

Author

van den Brink, Susanne C., Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, and Baillie-Johnson, Peter

Subjects
Embryonic development -- Analysis -- Methods -- Usage, RNA sequencing -- Usage, Embryonic stem cells -- Composition -- Usage -- Analysis -- Methods, Gastrulation -- Analysis -- Usage -- Methods, Somite -- Analysis -- Methods -- Usage, Genetic transcription -- Methods -- Usage -- Analysis, Environmental issues, Science and technology, Zoology and wildlife conservation
Abstract

Gastruloids are three-dimensional aggregates of embryonic stem cells that display key features of mammalian development after implantation, including germ-layer specification and axial organization.sup.1-3. To date, the expression pattern of only a small number of genes in gastruloids has been explored with microscopy, and the extent to which genome-wide expression patterns in gastruloids mimic those in embryos is unclear. Here we compare mouse gastruloids with mouse embryos using single-cell RNA sequencing and spatial transcriptomics. We identify various embryonic cell types that were not previously known to be present in gastruloids, and show that key regulators of somitogenesis are expressed similarly between embryos and gastruloids. Using live imaging, we show that the somitogenesis clock is active in gastruloids and has dynamics that resemble those in vivo. Because gastruloids can be grown in large quantities, we performed a small screen that revealed how reduced FGF signalling induces a short-tail phenotype in embryos. Finally, we demonstrate that embedding in Matrigel induces gastruloids to generate somites with the correct rostral-caudal patterning, which appear sequentially in an anterior-to-posterior direction over time. This study thus shows the power of gastruloids as a model system for exploring development and somitogenesis in vitro in a high-throughput manner. Single-cell RNA sequencing and spatial transcriptomics reveal that the somitogenesis clock is active in mouse gastruloids, which can be induced to generate somites with the correct rostral-caudal patterning., Author(s): Susanne C. van den Brink [sup.1] , Anna Alemany [sup.1] , Vincent van Batenburg [sup.1] , Naomi Moris [sup.2] , Marloes Blotenburg [sup.1] , Judith Vivié [sup.1] , Peter [...]

Published
2020
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8. Embryo-uterine interaction coordinates mouse embryogenesis during implantation

Author

00512477, Bondarenko, Vladyslav, Nikolaev, Mikhail, Kromm, Dimitri, Belousov, Roman, Wolny, Adrian, Blotenburg, Marloes, Zeller, Peter, Rezakhani, Saba, Hugger, Johannes, Uhlmann, Virginie, Hufnagel, Lars, Kreshuk, Anna, Ellenberg, Jan, van Oudenaarden, Alexander, Erzberger, Anna, Lutolf, Matthias P, Hiiragi, Takashi, 00512477, Bondarenko, Vladyslav, Nikolaev, Mikhail, Kromm, Dimitri, Belousov, Roman, Wolny, Adrian, Blotenburg, Marloes, Zeller, Peter, Rezakhani, Saba, Hugger, Johannes, Uhlmann, Virginie, Hufnagel, Lars, Kreshuk, Anna, Ellenberg, Jan, van Oudenaarden, Alexander, Erzberger, Anna, Lutolf, Matthias P, and Hiiragi, Takashi

Abstract

Embryo implantation into the uterus marks a key transition in mammalian development. In mice, implantation is mediated by the trophoblast and is accompanied by a morphological transition from the blastocyst to the egg cylinder. However, the roles of trophoblast‐uterine interactions in embryo morphogenesis during implantation are poorly understood due to inaccessibility in utero and the remaining challenges to recapitulate it ex vivo from the blastocyst. Here, we engineer a uterus‐like microenvironment to recapitulate peri‐implantation development of the whole mouse embryo ex vivo and reveal essential roles of the physical embryo‐uterine interaction. We demonstrate that adhesion between the trophoblast and the uterine matrix is required for in utero‐like transition of the blastocyst to the egg cylinder. Modeling the implanting embryo as a wetting droplet links embryo shape dynamics to the underlying changes in trophoblast adhesion and suggests that the adhesion‐mediated tension release facilitates egg cylinder formation. Light‐sheet live imaging and the experimental control of the engineered uterine geometry and trophoblast velocity uncovers the coordination between trophoblast motility and embryo growth, where the trophoblast delineates space for embryo morphogenesis.

Published
2023

9. Embryo-uterine interaction coordinates mouse embryogenesis during implantation

Author

CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, Bondarenko, Vladyslav, Nikolaev, Mikhail, Kromm, Dimitri, Belousov, Roman, Wolny, Adrian, Blotenburg, Marloes, Zeller, Peter, Rezakhani, Saba, Hugger, Johannes, Uhlmann, Virginie, Hufnagel, Lars, Kreshuk, Anna, Ellenberg, Jan, van Oudenaarden, Alexander, Erzberger, Anna, Lutolf, Matthias P., Hiiragi, Takashi, CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, Bondarenko, Vladyslav, Nikolaev, Mikhail, Kromm, Dimitri, Belousov, Roman, Wolny, Adrian, Blotenburg, Marloes, Zeller, Peter, Rezakhani, Saba, Hugger, Johannes, Uhlmann, Virginie, Hufnagel, Lars, Kreshuk, Anna, Ellenberg, Jan, van Oudenaarden, Alexander, Erzberger, Anna, Lutolf, Matthias P., and Hiiragi, Takashi

Published
2023

11. BMP gradient along the intestinal villus axis controls zonated enterocyte and goblet cell states

Author

Nefro Vasculaire Geneeskunde, Beumer, Joep, Puschhof, Jens, Yengej, Fjodor Yousef, Zhao, Lianzheng, Martinez-Silgado, Adriana, Blotenburg, Marloes, Begthel, Harry, Boot, Charelle, van Oudenaarden, Alexander, Chen, Ye Guang, Clevers, Hans, Nefro Vasculaire Geneeskunde, Beumer, Joep, Puschhof, Jens, Yengej, Fjodor Yousef, Zhao, Lianzheng, Martinez-Silgado, Adriana, Blotenburg, Marloes, Begthel, Harry, Boot, Charelle, van Oudenaarden, Alexander, Chen, Ye Guang, and Clevers, Hans

Published
2022

13. Activation of IRE1, PERK and salt-inducible kinases leads to Sec body formation in Drosophila S2 cells

Author

Zhang, Chujun, van Leeuwen, Wessel, Blotenburg, Marloes, Aguilera-Gomez, Angelica, Brussee, Sem, Grond, Rianne, Kampinga, Harm H, Rabouille, Catherine, Zhang, Chujun, van Leeuwen, Wessel, Blotenburg, Marloes, Aguilera-Gomez, Angelica, Brussee, Sem, Grond, Rianne, Kampinga, Harm H, and Rabouille, Catherine

Abstract

The phase separation of the non-membrane bound Sec bodies occurs in Drosophila S2 cells by coalescence of components of the endoplasmic reticulum (ER) exit sites under the stress of amino acid starvation. Here, we address which signaling pathways cause Sec body formation and find that two pathways are critical. The first is the activation of the salt-inducible kinases (SIKs; SIK2 and SIK3) by Na+ stress, which, when it is strong, is sufficient. The second is activation of IRE1 and PERK (also known as PEK in flies) downstream of ER stress induced by the absence of amino acids, which needs to be combined with moderate salt stress to induce Sec body formation. SIK, and IRE1 and PERK activation appear to potentiate each other through the stimulation of the unfolded protein response, a key parameter in Sec body formation. This work shows the role of SIKs in phase transition and re-enforces the role of IRE1 and PERK as a metabolic sensor for the level of circulating amino acids and salt. This article has an associated First Person interview with the first author of the paper.

Published
2021

14. Activation of IRE1, PERK and salt-inducible kinases leads to Sec body formation in Drosophila S2 cells

Author

Neurogenetica, CMM Groep Klumperman, CMM Sectie Celbiologie, Cancer, Hubrecht Institute with UMC, Zhang, Chujun, van Leeuwen, Wessel, Blotenburg, Marloes, Aguilera-Gomez, Angelica, Brussee, Sem, Grond, Rianne, Kampinga, Harm H., Rabouille, Catherine, Neurogenetica, CMM Groep Klumperman, CMM Sectie Celbiologie, Cancer, Hubrecht Institute with UMC, Zhang, Chujun, van Leeuwen, Wessel, Blotenburg, Marloes, Aguilera-Gomez, Angelica, Brussee, Sem, Grond, Rianne, Kampinga, Harm H., and Rabouille, Catherine

Published
2021

15. Activation of IRE1, PERK and salt-inducible kinases leads to Sec body formation in Drosophila S2 cells.

Author

Chujun Zhang, van Leeuwen, Wessel, Blotenburg, Marloes, Aguilera-Gomez, Angelica, Brussee, Sem, Grond, Rianne, Kampinga, Harm H., and Rabouille, Catherine

Subjects
UNFOLDED protein response, PHASE transitions, DROSOPHILA, KINASES, PHASE separation
Abstract

The phase separation of the non-membrane bound Sec bodies occurs in Drosophila S2 cells by coalescence of components of the endoplasmic reticulum (ER) exit sites under the stress of amino acid starvation. Here, we address which signaling pathways cause Sec body formation and find that two pathways are critical. The first is the activation of the salt-inducible kinases (SIKs; SIK2 and SIK3) by Na+ stress, which, when it is strong, is sufficient. The second is activation of IRE1 and PERK (also known as PEK in flies) downstream of ER stress induced by the absence of amino acids, which needs to be combined with moderate salt stress to induce Sec body formation. SIK, and IRE1 and PERK activation appear to potentiate each other through the stimulation of the unfolded protein response, a key parameter in Sec body formation. This work shows the role of SIKs in phase transition and re-enforces the role of IRE1 and PERK as a metabolic sensor for the level of circulating amino acids and salt. [ABSTRACT FROM AUTHOR]

Published
2022
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16. Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids

Author

van den Brink, Susanne C, Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F, Martinez Arias, Alfonso, van Oudenaarden, Alexander, van den Brink, Susanne C, Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F, Martinez Arias, Alfonso, and van Oudenaarden, Alexander

Abstract

Gastruloids are three-dimensional aggregates of embryonic stem cells that display key features of mammalian development after implantation, including germ-layer specification and axial organization1-3. To date, the expression pattern of only a small number of genes in gastruloids has been explored with microscopy, and the extent to which genome-wide expression patterns in gastruloids mimic those in embryos is unclear. Here we compare mouse gastruloids with mouse embryos using single-cell RNA sequencing and spatial transcriptomics. We identify various embryonic cell types that were not previously known to be present in gastruloids, and show that key regulators of somitogenesis are expressed similarly between embryos and gastruloids. Using live imaging, we show that the somitogenesis clock is active in gastruloids and has dynamics that resemble those in vivo. Because gastruloids can be grown in large quantities, we performed a small screen that revealed how reduced FGF signalling induces a short-tail phenotype in embryos. Finally, we demonstrate that embedding in Matrigel induces gastruloids to generate somites with the correct rostral-caudal patterning, which appear sequentially in an anterior-to-posterior direction over time. This study thus shows the power of gastruloids as a model system for exploring development and somitogenesis in vitro in a high-throughput manner.

Published
2020

17. Publisher Correction: Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids

Author

CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, van den Brink, Susanne C, Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F, Martinez Arias, Alfonso, van Oudenaarden, Alexander, CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, van den Brink, Susanne C, Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F, Martinez Arias, Alfonso, and van Oudenaarden, Alexander

Published
2020

18. Epigenetic priming by Dppa2 and 4 in pluripotency facilitates multi-lineage commitment

Author

Hubrecht Institute with UMC, Eckersley-Maslin, Mélanie A, Parry, Aled, Blotenburg, Marloes, Krueger, Christel, Ito, Yoko, Franklin, Valar Nila Roamio, Narita, Masashi, D'Santos, Clive S, Reik, Wolf, Hubrecht Institute with UMC, Eckersley-Maslin, Mélanie A, Parry, Aled, Blotenburg, Marloes, Krueger, Christel, Ito, Yoko, Franklin, Valar Nila Roamio, Narita, Masashi, D'Santos, Clive S, and Reik, Wolf

Published
2020

19. Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids

Author

CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, van den Brink, Susanne C., Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F., Martinez Arias, Alfonso, van Oudenaarden, Alexander, CMM Sectie Molecular Cancer Research, Cancer, Hubrecht Institute with UMC, van den Brink, Susanne C., Alemany, Anna, van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F., Martinez Arias, Alfonso, and van Oudenaarden, Alexander

Published
2020

25. Single-cell and spatial transcriptomics reveal somitogenesis in gastruloids

Author

Van Den Brink, Susanne C, Alemany, Anna, Van Batenburg, Vincent, Moris, Naomi, Blotenburg, Marloes, Vivié, Judith, Baillie-Johnson, Peter, Nichols, Jennifer, Sonnen, Katharina F, Martinez Arias, Alfonso, and Van Oudenaarden, Alexander

Subjects
Male, Time Factors, Embryonic Development, Gene Expression Regulation, Developmental, Mouse Embryonic Stem Cells, Gastrula, Embryo, Mammalian, 3. Good health, Organoids, Drug Combinations, Mice, Somites, Animals, Female, Proteoglycans, Collagen, Laminin, RNA-Seq, Single-Cell Analysis, Transcriptome
Abstract

Gastruloids are three-dimensional aggregates of embryonic stem cells that display key features of mammalian development after implantation, including germ-layer specification and axial organization1-3. To date, the expression pattern of only a small number of genes in gastruloids has been explored with microscopy, and the extent to which genome-wide expression patterns in gastruloids mimic those in embryos is unclear. Here we compare mouse gastruloids with mouse embryos using single-cell RNA sequencing and spatial transcriptomics. We identify various embryonic cell types that were not previously known to be present in gastruloids, and show that key regulators of somitogenesis are expressed similarly between embryos and gastruloids. Using live imaging, we show that the somitogenesis clock is active in gastruloids and has dynamics that resemble those in vivo. Because gastruloids can be grown in large quantities, we performed a small screen that revealed how reduced FGF signalling induces a short-tail phenotype in embryos. Finally, we demonstrate that embedding in Matrigel induces gastruloids to generate somites with the correct rostral-caudal patterning, which appear sequentially in an anterior-to-posterior direction over time. This study thus shows the power of gastruloids as a model system for exploring development and somitogenesis in vitro in a high-throughput manner.

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