Dissecting peri-implantation development using cultured human embryos and embryo-like assembloids

被引:46
作者
Ai, Zongyong [1 ,2 ,3 ]
Niu, Baohua [1 ,2 ]
Yin, Yu [1 ,2 ,3 ]
Xiang, Lifeng [4 ]
Shi, Gaohui [1 ,2 ]
Duan, Kui [1 ,2 ,3 ]
Wang, Sile [1 ,2 ,3 ]
Hu, Yingjie [1 ,2 ]
Zhang, Chi [1 ,2 ]
Zhang, Chengting [1 ,2 ,3 ]
Rong, Lujuan [1 ,2 ]
Kong, Ruize [4 ]
Chen, Tingwei [1 ,2 ]
Guo, Yixin [5 ]
Liu, Wanlu [5 ]
Li, Nan [1 ,2 ]
Zhao, Shumei [1 ,2 ,3 ]
Zhu, Xiaoqing [1 ,2 ,3 ]
Mai, Xuancheng [4 ]
Li, Yonggang [4 ]
Wu, Ze [4 ]
Zheng, Yi [6 ]
Fu, Jianping [6 ,7 ,8 ]
Ji, Weizhi [1 ,2 ,3 ]
Li, Tianqing [1 ,2 ,3 ]
机构
[1] Kunming Univ Sci & Technol, Inst Primate Translat Med, State Key Lab Primate Biomed Res, Kunming, Yunnan, Peoples R China
[2] Yunnan Key Lab Primate Biomed Res, Kunming, Yunnan, Peoples R China
[3] Yunnan Prov Acad Sci & Technol, Kunming, Yunnan, Peoples R China
[4] First Peoples Hosp Yunnan Prov, Dept Reprod Med, Kunming, Yunnan, Peoples R China
[5] Zhejiang Univ, Univ Edinburgh Inst, Sch Med, Int Campus,ZJU UoE Inst, Hangzhou, Zhejiang, Peoples R China
[6] Univ Michigan, Dept Mech Engn, Ann Arbor, MI USA
[7] Univ Michigan, Dept Biomed Engn, Ann Arbor, MI USA
[8] Univ Michigan, Med Sch, Dept Cell & Dev Biol, Ann Arbor, MI USA
基金
中国国家自然科学基金;
关键词
PLURIPOTENT STEM-CELLS; NAIVE PLURIPOTENCY; CLINICAL TRANSLATION; SELF-ORGANIZATION; STATE; MODEL; DIFFERENTIATION; IDENTIFICATION; ESTABLISHMENT; IMPLANTATION;
D O I
10.1038/s41422-023-00846-8
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Studies of cultured embryos have provided insights into human peri-implantation development. However, detailed knowledge of peri-implantation lineage development as well as underlying mechanisms remains obscure. Using 3D-cultured human embryos, herein we report a complete cell atlas of the early post-implantation lineages and decipher cellular composition and gene signatures of the epiblast and hypoblast derivatives. In addition, we develop an embryo-like assembloid (E-assembloid) by assembling naive hESCs and extraembryonic cells. Using human embryos and E-assembloids, we reveal that WNT, BMP and Nodal signaling pathways synergistically, but functionally differently, orchestrate human peri-implantation lineage development. Specially, we dissect mechanisms underlying extraembryonic mesoderm and extraembryonic endoderm specifications. Finally, an improved E-assembloid is developed to recapitulate the epiblast and hypoblast development and tissue architectures in the pre-gastrulation human embryo. Our findings provide insights into human peri-implantation development, and the E-assembloid offers a useful model to disentangle cellular behaviors and signaling interactions that drive human embryogenesis.
引用
收藏
页码:661 / 678
页数:18
相关论文
共 76 条
[1]   Deconstructing human peri-implantation embryogenesis based on embryos and embryoids† [J].
Ai, Zongyong ;
Yin, Yu ;
Niu, Baohua ;
Li, Tianqing .
BIOLOGY OF REPRODUCTION, 2022, 107 (01) :212-225
[2]   Modulation of Wnt and Activin/Nodal supports efficient derivation, cloning and suspension expansion of human pluripotent stem cells [J].
Ai, Zongyong ;
Niu, Baohua ;
Duan, Kui ;
Si, Chenyang ;
Wang, Sile ;
Xiang, Lifeng ;
Zhu, Xiaoqing ;
Zhu, Qingyuan ;
Feng, Chun ;
Yin, Yu ;
Zhao, Shumei ;
Kong, Ruize ;
Ji, Weizhi ;
Li, Tianqing .
BIOMATERIALS, 2020, 249
[3]   Overcoming Autocrine FGF Signaling-Induced Heterogeneity in Naive Human ESCs Enables Modeling of Random X Chromosome Inactivation [J].
An, Chenrui ;
Feng, Guihai ;
Zhang, Jixiang ;
Cao, Shiwei ;
Wang, Ying ;
Wang, Nannan ;
Lu, Falong ;
Zhou, Qi ;
Wang, Haoyi .
CELL STEM CELL, 2020, 27 (03) :482-+
[4]   Stem cell-derived synthetic embryos self-assemble by exploiting cadherin codes and cortical tension [J].
Bao, Min ;
Cornwall-Scoones, Jake ;
Sanchez-Vasquez, Estefania ;
Chen, Dong-Yuan ;
De Jonghe, Joachim ;
Shadkhoo, Shahriar ;
Hollfelder, Florian ;
Thomson, Matt ;
Glover, David M. ;
Zernicka-Goetz, Magdalena .
NATURE CELL BIOLOGY, 2022, 24 (09) :1341-+
[5]   Principles of signaling pathway modulation for enhancing human naive pluripotency induction [J].
Bayerl, Jonathan ;
Ayyash, Muneef ;
Shani, Tom ;
Manor, Yair Shlomo ;
Gafni, Ohad ;
Massarwa, Rada ;
Kalma, Yael ;
Aguilera-Castrejon, Alejandro ;
Zerbib, Mirie ;
Amir, Hadar ;
Sheban, Daoud ;
Geula, Shay ;
Mor, Nofar ;
Weinberger, Leehee ;
Tassa, Segev Naveh ;
Krupalnik, Vladislav ;
Oldak, Bernardo ;
Livnat, Nir ;
Tarazi, Shadi ;
Tawil, Shadi ;
Wildschutz, Emilie ;
Ashouokhi, Shahd ;
Lasman, Lior ;
Rotter, Varda ;
Hanna, Suhair ;
Ben-Yosef, Dalit ;
Novershtern, Noa ;
Viukov, Sergey ;
Hanna, Jacob H. .
CELL STEM CELL, 2021, 28 (09) :1549-+
[6]   Spatial profiling of early primate gastrulation in utero [J].
Bergmann, Sophie ;
Penfold, Christopher A. ;
Slatery, Erin ;
Siriwardena, Dylan ;
Drummer, Charis ;
Clark, Stephen ;
Strawbridge, Stanley E. ;
Kishimoto, Keiko ;
Vickers, Alice ;
Tewary, Mukul ;
Kohler, Timo N. ;
Hollfelder, Florian ;
Reik, Wolf ;
Sasaki, Erika ;
Behr, Rudiger ;
Boroviak, Thorsten E. .
NATURE, 2022, 609 (7925) :136-+
[7]   Identification of ALPPL2 as a Naive Pluripotent State-Specific Surface Protein Essential for Human Naive Pluripotency Regulation [J].
Bi, Yan ;
Tu, Zhifen ;
Zhang, Yanping ;
Yang, Peng ;
Guo, Mingyue ;
Zhu, Xuehao ;
Zhao, Chengchen ;
Zhou, Jianfeng ;
Wang, Hong ;
Wang, Yixuan ;
Gao, Shaorong .
CELL REPORTS, 2020, 30 (11) :3917-+
[8]   Defining the three cell lineages of the human blastocyst by single-cell RNA-seq (vol 142, pg 3151, 2015) [J].
Blakeley, Paul ;
Fogarty, Norah M. E. ;
del Valle, Ignacio ;
Wamaitha, Sissy E. ;
Hu, Tim Xiaoming ;
Elder, Kay ;
Snell, Philip ;
Christie, Leila ;
Robson, Paul ;
Niakan, Kathy K. .
DEVELOPMENT, 2015, 142 (20) :3613-3613
[9]   Single cell transcriptome analysis of human, marmoset and mouse embryos reveals common and divergent features of preimplantation development [J].
Boroviak, Thorsten ;
Stirparo, Giuliano G. ;
Dietmann, Sabine ;
Hernando-Herraez, Irene ;
Mohammed, Hisham ;
Reik, Wolf ;
Smith, Austin ;
Sasaki, Erika ;
Nichols, Jennifer ;
Bertone, Paul .
DEVELOPMENT, 2018, 145 (21)
[10]   Lineage-Specific Profiling Delineates the Emergence and Progression of Naive Pluripotency in Mammalian Embryogenesis [J].
Boroviak, Thorsten ;
Loos, Remco ;
Lombard, Patrick ;
Okahara, Junko ;
Behr, Ruediger ;
Sasaki, Erika ;
Nichols, Jennifer ;
Smith, Austin ;
Bertone, Paul .
DEVELOPMENTAL CELL, 2015, 35 (03) :366-382