Multi-axial self-organization properties of mouse embryonic stem cells into gastruloids

被引:326
作者
Beccari, Leonardo [1 ]
Moris, Naomi [2 ]
Girgin, Mehmet [3 ]
Turner, David A. [2 ]
Baillie-Johnson, Peter [2 ,5 ]
Cossy, Anne-Catherine [4 ]
Lutolf, Matthias P. [3 ]
Duboule, Denis [1 ,4 ]
Arias, Alfonso Martinez [2 ]
机构
[1] Univ Geneva, Dept Genet & Evolut, Geneva, Switzerland
[2] Univ Cambridge, Dept Genet, Cambridge, England
[3] Fed Inst Technol EPFL, Sch Life Sci, Lausanne, Switzerland
[4] Ecole Polytech Fed Lausanne, Swiss Canc Res Inst ISREC, Sch Life Sci, Lausanne, Switzerland
[5] Univ Cambridge, Wellcome Trust Med Res Council, Cambridge Stem Cell Inst, Cambridge, England
基金
欧洲研究理事会; 英国工程与自然科学研究理事会; 英国国家替代、减少和改良动物研究中心; 英国生物技术与生命科学研究理事会;
关键词
IN-VITRO; MORPHOGENESIS; DIFFERENTIATION; SPECIFICATION; ORGANOIDS; MAINTENANCE; EXPRESSION; PROGENITOR; INDUCTION; DYNAMICS;
D O I
10.1038/s41586-018-0578-0
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
070301 [无机化学]; 070403 [天体物理学]; 070507 [自然资源与国土空间规划学]; 090105 [作物生产系统与生态工程];
摘要
The emergence of multiple axes is an essential element in the establishment of the mammalian body plan. This process takes place shortly after implantation of the embryo within the uterus and relies on the activity of gene regulatory networks that coordinate transcription in space and time. Whereas genetic approaches have revealed important aspects of these processes(1), a mechanistic understanding is hampered by the poor experimental accessibility of early post-implantation stages. Here we show that small aggregates of mouse embryonic stem cells (ESCs), when stimulated to undergo gastrulation-like events and elongation in vitro, can organize a post-occipital pattern of neural, mesodermal and endodermal derivatives that mimic embryonic spatial and temporal gene expression. The establishment of the three major body axes in these 'gastruloids'(2,3) suggests that the mechanisms involved are interdependent. Specifically, gastruloids display the hallmarks of axial gene regulatory systems as exemplified by the implementation of collinear Hox transcriptional patterns along an extending anteroposterior axis. These results reveal an unanticipated self-organizing capacity of aggregated ESCs and suggest that gastruloids could be used as a complementary system to study early developmental events in the mammalian embryo.
引用
收藏
页码:272 / +
页数:21
相关论文
共 47 条
[1]
HTSeq-a Python']Python framework to work with high-throughput sequencing data [J].
Anders, Simon ;
Pyl, Paul Theodor ;
Huber, Wolfgang .
BIOINFORMATICS, 2015, 31 (02) :166-169
[2]
Generation of Aggregates of Mouse Embryonic Stem Cells that Show Symmetry Breaking, Polarization and Emergent Collective Behaviour In Vitro [J].
Baillie-Johnson, Peter ;
van den Brink, Susanne Carina ;
Balayo, Tina ;
Turner, David Andrew ;
Arias, Alfonso Martinez .
JOVE-JOURNAL OF VISUALIZED EXPERIMENTS, 2015, (105)
[3]
Beccari L., 2018, PROTOC EXCH, DOI DOI 10.1038/PROTEX.2018.094
[4]
EXPRESSION OF CDX-2 IN THE MOUSE EMBRYO AND PLACENTA - POSSIBLE ROLE IN PATTERNING OF THE EXTRAEMBRYONIC MEMBRANES [J].
BECK, F ;
ERLER, T ;
RUSSELL, A ;
JAMES, R .
DEVELOPMENTAL DYNAMICS, 1995, 204 (03) :219-227
[5]
Blankenberg Daniel, 2010, Curr Protoc Mol Biol, VChapter 19, DOI 10.1002/0471142727.mb1910s89
[6]
GASTRULATION IN THE MOUSE - THE ROLE OF THE HOMEOBOX GENE GOOSECOID [J].
BLUM, M ;
GAUNT, SJ ;
CHO, KWY ;
STEINBEISSER, H ;
BLUMBERG, B ;
BITTNER, D ;
DEROBERTIS, EM .
CELL, 1992, 69 (07) :1097-1106
[7]
The transcriptional landscape of the mammalian genome [J].
Carninci, P ;
Kasukawa, T ;
Katayama, S ;
Gough, J ;
Frith, MC ;
Maeda, N ;
Oyama, R ;
Ravasi, T ;
Lenhard, B ;
Wells, C ;
Kodzius, R ;
Shimokawa, K ;
Bajic, VB ;
Brenner, SE ;
Batalov, S ;
Forrest, ARR ;
Zavolan, M ;
Davis, MJ ;
Wilming, LG ;
Aidinis, V ;
Allen, JE ;
Ambesi-Impiombato, X ;
Apweiler, R ;
Aturaliya, RN ;
Bailey, TL ;
Bansal, M ;
Baxter, L ;
Beisel, KW ;
Bersano, T ;
Bono, H ;
Chalk, AM ;
Chiu, KP ;
Choudhary, V ;
Christoffels, A ;
Clutterbuck, DR ;
Crowe, ML ;
Dalla, E ;
Dalrymple, BP ;
de Bono, B ;
Della Gatta, G ;
di Bernardo, D ;
Down, T ;
Engstrom, P ;
Fagiolini, M ;
Faulkner, G ;
Fletcher, CF ;
Fukushima, T ;
Furuno, M ;
Futaki, S ;
Gariboldi, M .
SCIENCE, 2005, 309 (5740) :1559-1563
[8]
Recapitulating early development of mouse musculoskeletal precursors of the paraxial mesoderm in vitro [J].
Chal, Jerome ;
Al Tanoury, Ziad ;
Oginuma, Masayuki ;
Moncuquet, Philippe ;
Gobert, Benedicte ;
Miyanari, Ayako ;
Tassy, Olivier ;
Guevara, Getzabel ;
Hubaud, Alexis ;
Bera, Agata ;
Sumara, Olga ;
Garnier, Jean-Marie ;
Kennedy, Leif ;
Knockaert, Marie ;
Gayraud-Morel, Barbara ;
Tajbakhsh, Shahragim ;
Pourquie, Olivier .
DEVELOPMENT, 2018, 145 (06)
[9]
A role for mitotic bookmarking of SOX2 in pluripotency and differentiation [J].
Deluz, Cedric ;
Friman, Elias T. ;
Strebinger, Daniel ;
Benke, Alexander ;
Raccaud, Mahe ;
Callegari, Andrea ;
Leleu, Marion ;
Manley, Suliana ;
Suter, David M. .
GENES & DEVELOPMENT, 2016, 30 (22) :2538-2550
[10]
Developmental regulation of the Hox genes during axial morphogenesis in the mouse [J].
Deschamps, J ;
van Nes, J .
DEVELOPMENT, 2005, 132 (13) :2931-2942