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Developmental Biology May 2022
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Cell and Tissue Research Sep 2019Digestive systems and extracellular digestion are key animal features, but their emergence during early animal evolution is currently poorly understood. As the last... (Review)
Review
Digestive systems and extracellular digestion are key animal features, but their emergence during early animal evolution is currently poorly understood. As the last common ancestor of non-bilaterian animal groups (sponges, ctenophores, placozoans and cnidarians) dates back to the beginning of animal life, their study and comparison provides important insights into the early evolution of digestive systems and functions. Here, I have compiled an overview of the development and cell biology of digestive tissues in non-bilaterian animals. I will highlight the fundamental differences between extracellular and intracellular digestive processes, and how these are distributed among animals. Cnidarians (e.g. sea anemones, corals, jellyfish), the phylogenetic outgroup of bilaterians (e.g. vertebrates, flies, annelids), occupy a key position to reconstruct the evolution of bilaterian gut evolution. A major focus will therefore lie on the development and cell biology of digestive tissues in cnidarians, especially sea anemones, and how they compare to bilaterian gut tissues. In that context, I will also review how a recent study on the gastrula fate map of the sea anemone Nematostella vectensis challenges our long-standing conceptions on the evolution of cnidarian and bilaterian germ layers and guts.
Topics: Animals; Biological Evolution; Digestive System; Morphogenesis; Phylogeny; Sea Anemones
PubMed: 31388768
DOI: 10.1007/s00441-019-03075-x -
Developmental Cell Jun 2023Mesenchymal-epithelial transitions are fundamental drivers of development and disease, but how these behaviors generate epithelial structure is not well understood....
Mesenchymal-epithelial transitions are fundamental drivers of development and disease, but how these behaviors generate epithelial structure is not well understood. Here, we show that mesenchymal-epithelial transitions promote epithelial organization in the mouse node and notochordal plate through the assembly and radial intercalation of three-dimensional rosettes. Axial mesoderm rosettes acquire junctional and apical polarity, develop a central lumen, and dynamically expand, coalesce, and radially intercalate into the surface epithelium, converting mesenchymal-epithelial transitions into higher-order tissue structure. In mouse Par3 mutants, axial mesoderm rosettes establish central tight junction polarity but fail to form an expanded apical domain and lumen. These defects are associated with altered rosette dynamics, delayed radial intercalation, and formation of a small, fragmented surface epithelial structure. These results demonstrate that three-dimensional rosette behaviors translate mesenchymal-epithelial transitions into collective radial intercalation and epithelial formation, providing a strategy for building epithelial sheets from individual self-organizing units in the mammalian embryo.
Topics: Animals; Mice; Mesoderm; Epithelium; Cell Differentiation; Embryo, Mammalian; Morphogenesis; Mammals
PubMed: 37080203
DOI: 10.1016/j.devcel.2023.03.018 -
Developmental Cell Mar 2024Primordial germ cells (PGCs) are the earliest precursors of the gametes. During normal development, PGCs only give rise to oocytes or spermatozoa. However, PGCs can...
Primordial germ cells (PGCs) are the earliest precursors of the gametes. During normal development, PGCs only give rise to oocytes or spermatozoa. However, PGCs can acquire pluripotency in vitro by forming embryonic germ (EG) cells and in vivo during teratocarcinogenesis. Classic embryological experiments directly assessed the potency of PGCs by injection into the pre-implantation embryo. As no contribution to embryos or adult mice was observed, PGCs have been described as unipotent. Here, we demonstrate that PGCs injected into 8-cell embryos can initially survive, divide, and contribute to the developing inner cell mass. Apoptosis-deficient PGCs exhibit improved survival in isolated epiblasts and can form naive pluripotent embryonic stem cell lines. However, contribution to the post-implantation embryo is limited, with no functional incorporation observed. In contrast, PGC-like cells show an extensive contribution to mid-gestation chimeras. We thus propose that PGC formation in vivo establishes a latent form of pluripotency that restricts chimera contribution.
Topics: Male; Mice; Animals; Germ Cells; Embryonic Stem Cells; Pluripotent Stem Cells; Spermatozoa; Germ Layers; Cell Differentiation
PubMed: 38359835
DOI: 10.1016/j.devcel.2024.01.022 -
Cellular and Molecular Life Sciences :... May 2020Vertebrate cranial mesoderm is a discrete developmental unit compared to the mesoderm below the developing neck. An extraordinary feature of the cranial mesoderm is that... (Review)
Review
Vertebrate cranial mesoderm is a discrete developmental unit compared to the mesoderm below the developing neck. An extraordinary feature of the cranial mesoderm is that it includes a common progenitor pool contributing to the chambered heart and the craniofacial skeletal muscles. This striking developmental potential and the excitement it generated led to advances in our understanding of cranial mesoderm developmental mechanism. Remarkably, recent findings have begun to unravel the origin of its distinct developmental characteristics. Here, we take a detailed view of the ontogenetic trajectory of cranial mesoderm and its regulatory network. Based on the emerging evidence, we propose that cranial and posterior mesoderm diverge at the earliest step of the process that patterns the mesoderm germ layer along the anterior-posterior body axis. Further, we discuss the latest evidence and their impact on our current understanding of the evolutionary origin of cranial mesoderm. Overall, the review highlights the findings from contemporary research, which lays the foundation to probe the molecular basis of unique developmental potential and evolutionary origin of cranial mesoderm.
Topics: Animals; Biological Evolution; Gene Expression Regulation, Developmental; Humans; Mesoderm; Muscle Development; Muscle, Skeletal; Neural Crest; Skull; Vertebrates
PubMed: 31722070
DOI: 10.1007/s00018-019-03373-1 -
IScience Jan 2021Understanding the biological processes that determine the entry of three germ layers of human pluripotent stem cells (hPSCs) is a central question in developmental and...
Understanding the biological processes that determine the entry of three germ layers of human pluripotent stem cells (hPSCs) is a central question in developmental and stem cell biology. Here, we genetically engineered hPSCs with the germ layer reporter and inducible CRISPR/Cas9 knockout system, and a genome-scale screening was performed to define pathways restricting germ layer specification. Genes clustered in the key biological processes, including embryonic development, mRNA processing, metabolism, and epigenetic regulation, were centered in the governance of pluripotency and lineage development. Other than typical pluripotent transcription factors and signaling molecules, loss of function of mesendodermal specifiers resulted in advanced neuroectodermal differentiation, given their inter-germ layer antagonizing effect. Regarding the epigenetic superfamily, microRNAs enriched in hPSCs showed clear germ layer-targeting specificity. The cholesterol synthesis pathway maintained hPSCs via retardation of neuroectoderm specification. Thus, in this study, we identified a full landscape of genetic wiring and biological processes that control hPSC self-renewal and trilineage specification.
PubMed: 33385119
DOI: 10.1016/j.isci.2020.101926 -
Seminars in Cell & Developmental Biology Jul 2022The discovery of mesoderm inducing signals helped usher in the era of molecular developmental biology, and today the mechanisms of mesoderm induction and patterning are... (Review)
Review
The discovery of mesoderm inducing signals helped usher in the era of molecular developmental biology, and today the mechanisms of mesoderm induction and patterning are still intensely studied. Mesoderm induction begins during gastrulation, but recent evidence in vertebrates shows that this process continues after gastrulation in a group of posteriorly localized cells called neuromesodermal progenitors (NMPs). NMPs reside within the post-gastrulation embryonic structure called the tailbud, where they make a lineage decision between ectoderm (spinal cord) and mesoderm. The majority of NMP-derived mesoderm generates somites, but also contributes to lateral mesoderm fates such as endothelium. The discovery of NMPs provides a new paradigm in which to study vertebrate mesoderm induction. This review will discuss mechanisms of mesoderm induction within NMPs, and how they have informed our understanding of mesoderm induction more broadly within vertebrates as well as animal species outside of the vertebrate lineage. Special focus will be given to the signaling networks underlying NMP-derived mesoderm induction and patterning, as well as emerging work on the significance of partial epithelial-mesenchymal states in coordinating cell fate and morphogenesis.
Topics: Animals; Body Patterning; Cell Differentiation; Gastrulation; Gene Expression Regulation, Developmental; Mesoderm; Somites
PubMed: 34840081
DOI: 10.1016/j.semcdb.2021.11.010 -
Cell Cycle (Georgetown, Tex.) Nov 2019Mouse primordial germ cells (PGCs), originate from the early post-implantation epiblast in response to BMP4 secreted by the extraembryonic ectoderm. However, how BMP4... (Review)
Review
Mouse primordial germ cells (PGCs), originate from the early post-implantation epiblast in response to BMP4 secreted by the extraembryonic ectoderm. However, how BMP4 acts here has remained unclear. Recent work has identified the transcription factor (TF), OTX2 as a key determinant of the segregation of the germline from the soma. OTX2 is expressed ubiquitously in the early post-implantation epiblast, decreasing rapidly in cells that initiate the PGC programme. mRNA is also rapidly repressed by BMP4 , in germline competent cells. Supporting a model in which BMP4 represses , enforcing sustained OTX2 expression in competent cells blocks germline entry. In contrast, -null epiblast cells enter the germline with increased efficiency and and can do so independently of BMP4. Also, -null cells can initiate germline entry even without the crucial PGC TF, BLIMP1. In this review, we survey recent advances and propose hypotheses concerning germline entry.
Topics: Animals; Bone Morphogenetic Protein 4; Cell Differentiation; Ectoderm; Gene Expression Regulation, Developmental; Germ Cells; Germ Layers; Mice; Nanog Homeobox Protein; Otx Transcription Factors; Positive Regulatory Domain I-Binding Factor 1
PubMed: 31583942
DOI: 10.1080/15384101.2019.1672466 -
Genes Aug 2022Pluripotent stem cells (PSCs), which can self-renew and give rise to all cell types in all three germ layers, have great potential in regenerative medicine. Recent... (Review)
Review
Pluripotent stem cells (PSCs), which can self-renew and give rise to all cell types in all three germ layers, have great potential in regenerative medicine. Recent studies have shown that PSCs can have three distinct but interrelated pluripotent states: naive, formative, and primed. The PSCs of each state are derived from different stages of the early developing embryo and can be maintained in culture by different molecular mechanisms. In this review, we summarize the current understanding on features of the three pluripotent states and review the underlying molecular mechanisms of maintaining their identities. Lastly, we discuss the interrelation and transition among these pluripotency states. We believe that comprehending the divergence of pluripotent states is essential to fully harness the great potential of stem cells in regenerative medicine.
Topics: Animals; Embryo, Mammalian; Germ Layers; Humans; Mice; Pluripotent Stem Cells; Regenerative Medicine; Signal Transduction
PubMed: 36011370
DOI: 10.3390/genes13081459 -
Science Advances Jan 2024Spatiotemporal patterns widely occur in biological, chemical, and physical systems. Particularly, embryonic development displays a diverse gamut of repetitive patterns... (Review)
Review
Spatiotemporal patterns widely occur in biological, chemical, and physical systems. Particularly, embryonic development displays a diverse gamut of repetitive patterns established in many tissues and organs. Branching treelike structures in lungs, kidneys, livers, pancreases, and mammary glands as well as digits and bones in appendages, teeth, and palates are just a few examples. A fascinating instance of repetitive patterning is the sequential segmentation of the primary body axis, which is conserved in all vertebrates and many arthropods and annelids. In these species, the body axis elongates at the posterior end of the embryo containing an unsegmented tissue. Meanwhile, segments sequentially bud off from the anterior end of the unsegmented tissue, laying down an exquisite repetitive pattern and creating a segmented body plan. In vertebrates, the paraxial mesoderm is sequentially divided into somites. In this review, we will discuss the most prominent models, the most puzzling experimental data, and outstanding questions in vertebrate somite segmentation.
Topics: Animals; Body Patterning; Somites; Mesoderm; Vertebrates; Embryonic Development; Gene Expression Regulation, Developmental
PubMed: 38277458
DOI: 10.1126/sciadv.adk8937