The primitive streak and cellular principles of building an amniote body through gastrulation
The primitive streak and cellular principles of building an amniote body through gastrulation
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通过原肠胚形成羊膜体的原始条纹和细胞原理
DOI:
10.1126/science.abg1727
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发表时间:
2021
期刊:
影响因子:
56.9
通讯作者:
Sutherland Ann
中科院分区:
文献类型:
--
作者:
Sheng Guojun;Martinez Arias Alfonso;Sutherland Ann
BACKGROUNDPluripotent cells are generated by embryonic divisions that occur shortly after fertilization. These cells are transformed into the recognizable outline of an organism through the process of gastrulation, which endows them with lineage and spatial identities in the context of an emerging coordinate system. In many amniote embryos (such as those of reptiles, birds, and mammals), gastrulation has been associated with a transient structure called the primitive streak. Human development also follows this pattern. In humans, the primitive streak forms ~14 days after fertilization. The appearance of the primitive streak breaks the radial symmetry of the epiblast (a sheet of epithelialized pluripotent cells) and has been suggested to symbolize the emergence of human individuality. As such, many countries have established a legal limit of 14 days for the in vitro culture of fertilized human eggs—this is known as the “14-day rule.” In recent years, pluripotent stem cells have become a promising in vitro model for studying the cellular and molecular mechanisms associated with early human development. Interpretation of developmental features observed in these in vitro models requires proper understanding of animal gastrulation in general and of the amniote primitive streak in particular.ADVANCESIn this Review, we offer a phylogenetic and ontogenetic overview of the primitive streak and its role in mediating amniote gastrulation, and we discuss the implications of embryonic stem cell–based models of early mammalian embryogenesis on the function of this iconic structure. We provide evidence that the primitive streak is not a conserved feature in amniote development and that the mammalian and avian primitive streaks have evolved independently through different supracellular mechanisms that led to their morphological emergence. We argue that, in addition to mediating the emergence of germ layers from the pluripotent epiblast, gastrulation is principally a process in which an embryo acquires a coordinate system to organize its primary cell fates and the primordia of organs and tissues relative to each other in space. We highlight that in amniotes this process is regulated by a set of conserved signaling and transcriptional networks through a small collection of cellular behaviors, the tissue-level effects of which are governed by boundary conditions. We suggest that changing boundary conditions, in the form of evolution of extraembryonic lineages such as the trophectoderm and primitive endoderm, have played a key role in the transformation of the blastopore, characteristic of anamniote embryos, into the primitive streak. Variability in the organization of these tissues and the demarcation of embryonic and extraembryonic territories underpins the observed variation in the morphological appearance of the primitive streak in mammals and birds and of primitive streak–related structures in reptiles. Over the past few years, embryonic stem cells have been used as models to recapitulate several aspects of early mammalian embryogenesis. These studies have revealed that the germ layers, and even a rudimentary body plan, can form in the absence of a primitive streak.OUTLOOKOur model predicts that the most fundamental feature of a primitive streak–like structure in early amniote development is not its morphological manifestation but rather its capacity to mediate coordinated cell fate specification events in space. Our model also suggests that cell fate specification and tissue-level morphogenesis are regulated independently during gastrulation and then coordinated during embryonic development in vivo. In developmental models in vitro, these two …
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影响因子:
16.6
作者:
Xu PF;Borges RM;Fillatre J;de Oliveira-Melo M;Cheng T;Thisse B;Thisse C
通讯作者:
Thisse C
影响因子:
3.7
作者:
Coolen M;Nicolle D;Plouhinec JL;Gombault A;Sauka-Spengler T;Menuet A;Pieau C;Mazan S
通讯作者:
Mazan S
DOI:
10.1002/jez.b.21198
发表时间:
2008
期刊:
Journal of experimental zoology. Part B, Molecular and developmental evolution
影响因子:
--
作者:
Shook,DavidR;Keller,Ray
通讯作者:
Keller,Ray
DOI:
10.1159/000147748
发表时间:
1995
期刊:
Acta anatomica
影响因子:
--
作者:
E. Hay
通讯作者:
E. Hay
DOI:
10.1242/dev.111583
发表时间:
2015-01-01
期刊:
Development (Cambridge, England)
影响因子:
--
作者:
Stankova V;Tsikolia N;Viebahn C
通讯作者:
Viebahn C