Embryo-uterine interaction coordinates mouse embryogenesis during implantation

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

doi:10.15252/embj.2022113280

Embryo-uterine interaction coordinates mouse embryogenesis during implantation

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

Hubrecht Institute

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

6 Citations (Scopus)

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.

Original language	English
Pages (from-to)	e113280
Journal	EMBO Journal
Volume	42
Issue number	17
DOIs	https://doi.org/10.15252/embj.2022113280
Publication status	Published - 04 Sept 2023

Keywords

Female
Mice
Animals
Embryo Implantation
Blastocyst
Trophoblasts
Uterus
Embryonic Development
Mammals

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10.15252/embj.2022113280

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Bondarenko, V., Nikolaev, M., Kromm, D., Belousov, R., Wolny, A., Blotenburg, M., Zeller, P., Rezakhani, S., Hugger, J., Uhlmann, V., Hufnagel, L., Kreshuk, A., Ellenberg, J., van Oudenaarden, A., Erzberger, A., Lutolf, M. P., & Hiiragi, T. (2023). Embryo-uterine interaction coordinates mouse embryogenesis during implantation. EMBO Journal, 42(17), e113280. https://doi.org/10.15252/embj.2022113280

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title = "Embryo-uterine interaction coordinates mouse embryogenesis during implantation",

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.",

keywords = "Female, Mice, Animals, Embryo Implantation, Blastocyst, Trophoblasts, Uterus, Embryonic Development, Mammals",

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

note = "{\textcopyright} 2023 The Authors. Published under the terms of the CC BY 4.0 license.",

year = "2023",

month = sep,

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doi = "10.15252/embj.2022113280",

language = "English",

volume = "42",

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Bondarenko, V, Nikolaev, M, Kromm, D, Belousov, R, Wolny, A, Blotenburg, M, Zeller, P, Rezakhani, S, Hugger, J, Uhlmann, V, Hufnagel, L, Kreshuk, A, Ellenberg, J, van Oudenaarden, A, Erzberger, A, Lutolf, MP & Hiiragi, T 2023, 'Embryo-uterine interaction coordinates mouse embryogenesis during implantation', EMBO Journal, vol. 42, no. 17, pp. e113280. https://doi.org/10.15252/embj.2022113280

TY - JOUR

T1 - Embryo-uterine interaction coordinates mouse embryogenesis during implantation

AU - Bondarenko, Vladyslav

AU - Nikolaev, Mikhail

AU - Kromm, Dimitri

AU - Belousov, Roman

AU - Wolny, Adrian

AU - Blotenburg, Marloes

AU - Zeller, Peter

AU - Rezakhani, Saba

AU - Hugger, Johannes

AU - Uhlmann, Virginie

AU - Hufnagel, Lars

AU - Kreshuk, Anna

AU - Ellenberg, Jan

AU - van Oudenaarden, Alexander

AU - Erzberger, Anna

AU - Lutolf, Matthias P

AU - Hiiragi, Takashi

PY - 2023/9/4

Y1 - 2023/9/4

N2 - 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.

AB - 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.

KW - Female

KW - Mice

KW - Animals

KW - Embryo Implantation

KW - Blastocyst

KW - Trophoblasts

KW - Uterus

KW - Embryonic Development

KW - Mammals

U2 - 10.15252/embj.2022113280

DO - 10.15252/embj.2022113280

M3 - Article

C2 - 37522872

SN - 0261-4189

VL - 42

SP - e113280

JO - EMBO Journal

JF - EMBO Journal

IS - 17

ER -

Embryo-uterine interaction coordinates mouse embryogenesis during implantation

Abstract

Keywords

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