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Science (New York, N.Y.) Dec 2021The primitive streak, a transient embryonic structure, marks bilateral symmetry in mammalian and avian embryos and helps confer anterior-posterior and dorsal-ventral... (Review)
Review
The primitive streak, a transient embryonic structure, marks bilateral symmetry in mammalian and avian embryos and helps confer anterior-posterior and dorsal-ventral spatial information to early differentiating cells during gastrulation. Its recapitulation in vitro may facilitate derivation of tissues and organs with in vivo–like complexity. Proper understanding of the primitive streak and what it entails in human development is key to achieving such research objectives. Here we provide an overview of the primitive streak and conclude that this structure is neither conserved nor necessary for gastrulation or early lineage diversification. We offer a model in which the primitive streak is viewed as part of a morphologically diverse yet molecularly conserved process of spatial coordinate acquisition. We predict that recapitulation of the primitive streak is dispensable for development in vitro.
Topics: Animals; Biological Evolution; Embryo, Mammalian; Embryo, Nonmammalian; Gastrulation; Gene Expression Regulation, Developmental; Humans; Morphogenesis; Phylogeny; Primitive Streak; Vertebrates
PubMed: 34855481
DOI: 10.1126/science.abg1727 -
Anatomy and Embryology 1986The emphasis of this review is on the primitive streak of the chick embryo, collated with such information as is available on the mouse embryo. Little modern work has... (Comparative Study)
Comparative Study Review
The emphasis of this review is on the primitive streak of the chick embryo, collated with such information as is available on the mouse embryo. Little modern work has been published on any reptile primitive streak. The following topics are considered: evolutionary significance; formation of the primitive streak; ingression and de-epithelialisation; the basal lamina; migration from the primitive streak of the endoderm and mesoderm; the role of the extracellular matrix; changes in cell adhesiveness; regression of the primitive streak and its role in body patterning; the primitive streak and induction.
Topics: Animals; Basement Membrane; Biological Evolution; Cell Adhesion; Cell Movement; Chick Embryo; Ectoderm; Embryonic Induction; Epithelial Cells; Epithelium; Gastrula; Mesoderm; Mice; Rabbits; Species Specificity
PubMed: 3518538
DOI: 10.1007/BF00318331 -
Wiley Interdisciplinary Reviews.... Mar 2017In the animal kingdom, gastrulation, the process by which the primary germ layers are formed involves a dramatic transformation in the topology of the cells that give... (Review)
Review
In the animal kingdom, gastrulation, the process by which the primary germ layers are formed involves a dramatic transformation in the topology of the cells that give rise to all of the tissues of the adult. Initially formed as a mono-layer, this tissue, the epiblast, becomes subdivided through the internalization of cells, thereby forming a two (bi-laminar) or three (tri-laminar) layered embryo. This morphogenetic process coordinates the development of the fundamental body plan and the three-body axes (antero-posterior, dorso-ventral, and left-right) and begins a fundamental segregation of cells toward divergent developmental fates. In humans and other mammals, as well as in avians, gastrulating cells internalize along a structure, called the primitive streak, which builds from the periphery toward the center of the embryo. How these morphogenetic movements are orchestrated and evolved has been a question for developmental biologists for many years. Is the primitive streak a feature shared by the whole amniote clade? Insights from reptiles suggest that the primitive streak arose independently in mammals and avians, while the reptilian internalization site is a structure half-way between an amphibian blastopore and a primitive streak. The molecular machinery driving primitive streak formation has been partially dissected using mainly the avian embryo, revealing a paramount role of the planar cell polarity (PCP) pathway in streak formation. How did the employment of this machinery evolve? The reptilian branch of the amniote clade might provide us with useful tools to investigate the evolution of the amniote internalization site up to the formation of the primitive streak. WIREs Dev Biol 2017, 6:e262. doi: 10.1002/wdev.262 For further resources related to this article, please visit the WIREs website.
Topics: Amnion; Animals; Biological Evolution; Gastrula; Gastrulation; Germ Layers; Humans; Morphogenesis; Primitive Streak
PubMed: 28177589
DOI: 10.1002/wdev.262 -
Nature Jan 2020Our understanding of how human embryos develop before gastrulation, including spatial self-organization and cell type ontogeny, remains limited by available...
Our understanding of how human embryos develop before gastrulation, including spatial self-organization and cell type ontogeny, remains limited by available two-dimensional technological platforms that do not recapitulate the in vivo conditions. Here we report a three-dimensional (3D) blastocyst-culture system that enables human blastocyst development up to the primitive streak anlage stage. These 3D embryos mimic developmental landmarks and 3D architectures in vivo, including the embryonic disc, amnion, basement membrane, primary and primate unique secondary yolk sac, formation of anterior-posterior polarity and primitive streak anlage. Using single-cell transcriptome profiling, we delineate ontology and regulatory networks that underlie the segregation of epiblast, primitive endoderm and trophoblast. Compared with epiblasts, the amniotic epithelium shows unique and characteristic phenotypes. After implantation, specific pathways and transcription factors trigger the differentiation of cytotrophoblasts, extravillous cytotrophoblasts and syncytiotrophoblasts. Epiblasts undergo a transition to pluripotency upon implantation, and the transcriptome of these cells is maintained until the generation of the primitive streak anlage. These developmental processes are driven by different pluripotency factors. Together, findings from our 3D-culture approach help to determine the molecular and morphogenetic developmental landscape that occurs during human embryogenesis.
Topics: Amnion; Blastocyst; Cell Culture Techniques; Cell Differentiation; Cell Lineage; Cell Polarity; Collagen; Drug Combinations; Embryo, Mammalian; Embryonic Development; Epithelium; Gastrulation; Germ Layers; Humans; Laminin; Primitive Streak; Proteoglycans; RNA-Seq; Single-Cell Analysis; Transcription Factors; Transcriptome; Trophoblasts; Yolk Sac
PubMed: 31830756
DOI: 10.1038/s41586-019-1875-y -
Nature Feb 2019Across the animal kingdom, gastrulation represents a key developmental event during which embryonic pluripotent cells diversify into lineage-specific precursors that...
Across the animal kingdom, gastrulation represents a key developmental event during which embryonic pluripotent cells diversify into lineage-specific precursors that will generate the adult organism. Here we report the transcriptional profiles of 116,312 single cells from mouse embryos collected at nine sequential time points ranging from 6.5 to 8.5 days post-fertilization. We construct a molecular map of cellular differentiation from pluripotency towards all major embryonic lineages, and explore the complex events involved in the convergence of visceral and primitive streak-derived endoderm. Furthermore, we use single-cell profiling to show that Tal1 chimeric embryos display defects in early mesoderm diversification, and we thus demonstrate how combining temporal and transcriptional information can illuminate gene function. Together, this comprehensive delineation of mammalian cell differentiation trajectories in vivo represents a baseline for understanding the effects of gene mutations during development, as well as a roadmap for the optimization of in vitro differentiation protocols for regenerative medicine.
Topics: Animals; Cell Differentiation; Cell Lineage; Chimera; Embryo, Mammalian; Endoderm; Endothelium; Female; Gastrulation; Gene Expression Profiling; Gene Expression Regulation, Developmental; Hematopoiesis; Male; Mesoderm; Mice; Mutation; Myeloid Cells; Organogenesis; Pluripotent Stem Cells; Primitive Streak; Single-Cell Analysis; T-Cell Acute Lymphocytic Leukemia Protein 1
PubMed: 30787436
DOI: 10.1038/s41586-019-0933-9 -
Cell Stem Cell Jun 2023Gastruloids are 3D structures generated from pluripotent stem cells recapitulating fundamental principles of embryonic pattern formation. Using single-cell genomic...
Gastruloids are 3D structures generated from pluripotent stem cells recapitulating fundamental principles of embryonic pattern formation. Using single-cell genomic analysis, we provide a resource mapping cell states and types during gastruloid development and compare them with the in vivo embryo. We developed a high-throughput handling and imaging pipeline to spatially monitor symmetry breaking during gastruloid development and report an early spatial variability in pluripotency determining a binary response to Wnt activation. Although cells in the gastruloid-core revert to pluripotency, peripheral cells become primitive streak-like. These two populations subsequently break radial symmetry and initiate axial elongation. By performing a compound screen, perturbing thousands of gastruloids, we derive a phenotypic landscape and infer networks of genetic interactions. Finally, using a dual Wnt modulation, we improve the formation of anterior structures in the existing gastruloid model. This work provides a resource to understand how gastruloids develop and generate complex patterns in vitro.
Topics: Mice; Animals; Embryo, Mammalian; Primitive Streak; Pluripotent Stem Cells; Embryonic Development
PubMed: 37209681
DOI: 10.1016/j.stem.2023.04.018 -
Wiley Interdisciplinary Reviews.... Mar 2020In Placentalia, the fetus depends upon an organized vascular connection with its mother for survival and development. Yet, this connection was, until recently, obscure.... (Review)
Review
In Placentalia, the fetus depends upon an organized vascular connection with its mother for survival and development. Yet, this connection was, until recently, obscure. Here, we summarize how two unrelated tissues, the primitive streak, or body axis, and extraembryonic visceral endoderm collaborate to create and organize the fetal-placental arterial connection in the mouse gastrula. The primitive streak reaches into the extraembryonic space, where it marks the site of arterial union and creates a progenitor cell pool. Through contact with the streak, associated visceral endoderm undergoes an epithelial-to-mesenchymal transition, contributing extraembryonic mesoderm to the placental arterial vasculature, and to the allantois, or pre-umbilical tissue. In addition, visceral endoderm bifurcates into the allantois where, with the primitive streak, it organizes the nascent umbilical artery and promotes allantoic elongation to the chorion, the site of fetal-maternal exchange. Brachyury mediates streak extension and vascular patterning, while Hedgehog is involved in visceral endoderm's conversion to mesoderm. A unique CASPASE-3-positive cell separates streak- and non-streak-associated domains in visceral endoderm. Based on these new insights at the posterior embryonic-extraembryonic interface, we conclude by asking whether so-called primordial germ cells are truly antecedents to the germ line that segregate within the allantois, or whether they are placental progenitor cells. Incorporating these new working hypotheses into mutational analyses in which the placentae are affected will aid understanding a spectrum of disorders, including orphan diseases, which often include abnormalities of the umbilical cord, yolk sac, and hindgut, whose developmental relationship to each other has, until now, been poorly understood. This article is categorized under: Birth Defects > Associated with Preimplantation and Gastrulation Early Embryonic Development > Gastrulation and Neurulation.
Topics: Animals; Arteries; Embryo, Mammalian; Endoderm; Female; Fetus; Gastrula; Humans; Mice; Placenta; Pregnancy; Primitive Streak
PubMed: 31622045
DOI: 10.1002/wdev.362 -
Science (New York, N.Y.) Jul 1883
PubMed: 17733855
DOI: 10.1126/science.ns-2.25.105-b -
Science (New York, N.Y.) Mar 2021
Topics: Cell Differentiation; Cell Movement; Embryo Research; Ethics, Research; Gastrulation; Germ Layers; Guidelines as Topic; Humans; Primitive Streak
PubMed: 33674483
DOI: 10.1126/science.abf3751 -
BioEssays : News and Reviews in... Aug 2009The primitive streak establishes the antero-posterior body axis in all amniote species. It is thought to be the conduit through which mesoderm and endoderm progenitors... (Review)
Review
The primitive streak establishes the antero-posterior body axis in all amniote species. It is thought to be the conduit through which mesoderm and endoderm progenitors ingress and migrate to their ultimate destinations. Despite its importance, the streak remains poorly defined and one of the most enigmatic structures of the animal kingdom. In particular, the posterior end of the primitive streak has not been satisfactorily identified in any species. Unexpectedly, and contrary to prevailing notions, recent evidence suggests that the murine posterior primitive streak extends beyond the embryo proper. In its extraembryonic site, the streak creates a node-like cell reservoir from which the allantois, a universal caudal appendage of all amniotes and the future umbilical cord of placental mammals, emerges. This new insight into the fetal/umbilical relationship may explain the etiology of a large number of umbilical-associated birth defects, many of which are correlated with abnormalities of the embryonic midline.
Topics: Allantois; Animals; Body Patterning; Mammals; Mesoderm; Primitive Streak; Stem Cells
PubMed: 19609969
DOI: 10.1002/bies.200900038