Dissecting embryonic and extraembryonic lineage crosstalk with stem cell co-culture

Yulei Wei; E Zhang; Leqian Yu; Baiquan Ci; Masahiro Sakurai; Lei Guo; Xin Zhang; Sirui Lin; Shino Takii; Lizhong Liu; Jian Liu; Daniel A Schmitz; Ting Su; Junmei Zhang; Qiaoyan Shen; Yi Ding; Linfeng Zhan; Hai-Xi Sun; Canbin Zheng; Lin Xu; Daiji Okamura; Weizhi Ji; Tao Tan; Jun Wu

doi:10.1016/j.cell.2023.11.008

Dissecting embryonic and extraembryonic lineage crosstalk with stem cell co-culture

Cell. 2023 Dec 21;186(26):5859-5875.e24. doi: 10.1016/j.cell.2023.11.008. Epub 2023 Dec 4.

Authors

Yulei Wei¹, E Zhang², Leqian Yu³, Baiquan Ci², Masahiro Sakurai⁴, Lei Guo⁵, Xin Zhang⁶, Sirui Lin⁶, Shino Takii⁷, Lizhong Liu⁴, Jian Liu², Daniel A Schmitz⁴, Ting Su², Junmei Zhang⁸, Qiaoyan Shen⁹, Yi Ding⁴, Linfeng Zhan², Hai-Xi Sun¹⁰, Canbin Zheng⁴, Lin Xu⁵, Daiji Okamura⁷, Weizhi Ji¹¹, Tao Tan¹², Jun Wu¹³

Affiliations

¹ Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; State Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China. Electronic address: yulei.wei@cau.edu.cn.
² State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan 650500, China.
³ Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing 100101, China; Beijing Institute for Stem Cell and Regenerative Medicine, Beijing 100101, China.
⁴ Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
⁵ Quantitative Biomedical Research Center, Peter O'Donnell Jr. School of Public Health, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
⁶ State Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
⁷ Department of Advanced Bioscience, Graduate School of Agriculture, Kindai University, Nakamachi, Nara 631-8505, Japan.
⁸ State Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural University, Beijing 100193, China; State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing 100101, China.
⁹ State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing 100101, China.
¹⁰ BGI Research, Beijing 102601, China.
¹¹ State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan 650500, China. Electronic address: wji@lpbr.cn.
¹² State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Yunnan 650500, China. Electronic address: tant@lpbr.cn.
¹³ Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Cecil H. and Ida Green Center for Reproductive Biology Sciences, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA. Electronic address: jun2.wu@utsouthwestern.edu.

PMID: 38052213
PMCID: PMC10916932 (available on 2024-12-21)
DOI: 10.1016/j.cell.2023.11.008

Abstract

Embryogenesis necessitates harmonious coordination between embryonic and extraembryonic tissues. Although stem cells of both embryonic and extraembryonic origins have been generated, they are grown in different culture conditions. In this study, utilizing a unified culture condition that activates the FGF, TGF-β, and WNT pathways, we have successfully derived embryonic stem cells (FTW-ESCs), extraembryonic endoderm stem cells (FTW-XENs), and trophoblast stem cells (FTW-TSCs) from the three foundational tissues of mouse and cynomolgus monkey (Macaca fascicularis) blastocysts. This approach facilitates the co-culture of embryonic and extraembryonic stem cells, revealing a growth inhibition effect exerted by extraembryonic endoderm cells on pluripotent cells, partially through extracellular matrix signaling. Additionally, our cross-species analysis identified both shared and unique transcription factors and pathways regulating FTW-XENs. The embryonic and extraembryonic stem cell co-culture strategy offers promising avenues for developing more faithful embryo models and devising more developmentally pertinent differentiation protocols.

Keywords: ECM signaling; embryonic stem cell; extraembryonic endoderm stem cell; lineage crosstalk; monkey; mouse; trophoblast stem cell.

MeSH terms

Animals
Cell Differentiation
Cell Lineage
Coculture Techniques
Embryo, Mammalian*
Embryonic Stem Cells* / metabolism
Endoderm / metabolism
Macaca fascicularis

Abstract

MeSH terms

Grants and funding