Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs

Abstract Extraembryonic mesoderm (ExM) is crucial for human development, yet its specification is poorly understood. Human embryonic stem cell (hESC)-based models, including embryoids and differentiated derivatives, are emerging as promising tools for studying ExM development. Despite this, the sign...

Full description

Saved in:
Bibliographic Details
Main Authors: Baohua Niu, Da Wang, Yingjie Hu, Yundi Wang, Gaohui Shi, Zhongying Chen, Lifeng Xiang, Chi Zhang, Xuesong Wei, Ruize Kong, Hongzhi Cai, Weizhi Ji, Yu Yin, Tianqing Li, Zongyong Ai
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59491-x
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850268667655225344
author Baohua Niu
Da Wang
Yingjie Hu
Yundi Wang
Gaohui Shi
Zhongying Chen
Lifeng Xiang
Chi Zhang
Xuesong Wei
Ruize Kong
Hongzhi Cai
Weizhi Ji
Yu Yin
Tianqing Li
Zongyong Ai
author_facet Baohua Niu
Da Wang
Yingjie Hu
Yundi Wang
Gaohui Shi
Zhongying Chen
Lifeng Xiang
Chi Zhang
Xuesong Wei
Ruize Kong
Hongzhi Cai
Weizhi Ji
Yu Yin
Tianqing Li
Zongyong Ai
author_sort Baohua Niu
collection DOAJ
description Abstract Extraembryonic mesoderm (ExM) is crucial for human development, yet its specification is poorly understood. Human embryonic stem cell (hESC)-based models, including embryoids and differentiated derivatives, are emerging as promising tools for studying ExM development. Despite this, the signaling mechanisms and developmental dynamics that underlie ExM specification from hESCs remain challenging to study. Here, we report that the modulation of BMP, WNT, and Nodal signaling pathways can rapidly (4-5 days) and efficiently ( ~90%) induce the differentiation of both naive and primed hESCs into ExM-like cells (ExMs). We reveal that ExM specification from hESCs predominantly proceeds through intermediates exhibiting a primitive streak (PS)-like gene expression pattern and delineate the regulatory roles of WNT and Nodal signaling in this process. Furthermore, we find that the initial pluripotent state governs hESC-based ExM specification by influencing signal response, cellular composition, developmental progression, and transcriptional characteristics of the resulting ExMs. Our study provides promising models for dissecting human ExM development and sheds light on the signaling principles, developmental dynamics, and influences of pluripotency states underlying ExM specification from hESCs.
format Article
id doaj-art-09f89752e0bf446c8d7b6d2f2adde5dd
institution OA Journals
issn 2041-1723
language English
publishDate 2025-05-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-09f89752e0bf446c8d7b6d2f2adde5dd2025-08-20T01:53:23ZengNature PortfolioNature Communications2041-17232025-05-0116112010.1038/s41467-025-59491-xDeciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCsBaohua Niu0Da Wang1Yingjie Hu2Yundi Wang3Gaohui Shi4Zhongying Chen5Lifeng Xiang6Chi Zhang7Xuesong Wei8Ruize Kong9Hongzhi Cai10Weizhi Ji11Yu Yin12Tianqing Li13Zongyong Ai14State Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyUltrasound Department, The Third People’s Hospital of Yunnan ProvinceDepartment of Reproductive Medicine, The First People’s Hospital of Yunnan ProvinceState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyDepartment of Reproductive Medicine, The First People’s Hospital of Yunnan ProvinceState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyState Key Laboratory of Primate Biomedical Research; Institute of Primate Translational Medicine, Kunming University of Science and TechnologyAbstract Extraembryonic mesoderm (ExM) is crucial for human development, yet its specification is poorly understood. Human embryonic stem cell (hESC)-based models, including embryoids and differentiated derivatives, are emerging as promising tools for studying ExM development. Despite this, the signaling mechanisms and developmental dynamics that underlie ExM specification from hESCs remain challenging to study. Here, we report that the modulation of BMP, WNT, and Nodal signaling pathways can rapidly (4-5 days) and efficiently ( ~90%) induce the differentiation of both naive and primed hESCs into ExM-like cells (ExMs). We reveal that ExM specification from hESCs predominantly proceeds through intermediates exhibiting a primitive streak (PS)-like gene expression pattern and delineate the regulatory roles of WNT and Nodal signaling in this process. Furthermore, we find that the initial pluripotent state governs hESC-based ExM specification by influencing signal response, cellular composition, developmental progression, and transcriptional characteristics of the resulting ExMs. Our study provides promising models for dissecting human ExM development and sheds light on the signaling principles, developmental dynamics, and influences of pluripotency states underlying ExM specification from hESCs.https://doi.org/10.1038/s41467-025-59491-x
spellingShingle Baohua Niu
Da Wang
Yingjie Hu
Yundi Wang
Gaohui Shi
Zhongying Chen
Lifeng Xiang
Chi Zhang
Xuesong Wei
Ruize Kong
Hongzhi Cai
Weizhi Ji
Yu Yin
Tianqing Li
Zongyong Ai
Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
Nature Communications
title Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
title_full Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
title_fullStr Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
title_full_unstemmed Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
title_short Deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hESCs
title_sort deciphering signaling mechanisms and developmental dynamics in extraembryonic mesoderm specification from hescs
url https://doi.org/10.1038/s41467-025-59491-x
work_keys_str_mv AT baohuaniu decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT dawang decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT yingjiehu decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT yundiwang decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT gaohuishi decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT zhongyingchen decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT lifengxiang decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT chizhang decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT xuesongwei decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT ruizekong decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT hongzhicai decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT weizhiji decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT yuyin decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT tianqingli decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs
AT zongyongai decipheringsignalingmechanismsanddevelopmentaldynamicsinextraembryonicmesodermspecificationfromhescs