Growing an Embryo from a Single Cell: A Hurdle in Animal Life
TL;DR: In mammals and in endoparasites, development in a nutritive environment releases the growth constraint, but growth of cells before gastrulation requires a new program to sustain pluripotency during this growth.
Abstract: A requirement that an animal be able to feed to grow constrains how a cell can grow into an animal, and it forces an alternation between growth (increase in mass) and proliferation (increase in cell number). A growth-only phase that transforms a stem cell of ordinary proportions into a huge cell, the oocyte, requires dramatic adaptations to help a nucleus direct a 10(5)-fold expansion of cytoplasmic volume. Proliferation without growth transforms the huge egg into an embryo while still accommodating an impotent nucleus overwhelmed by the voluminous cytoplasm. This growth program characterizes animals that deposit their eggs externally, but it is changed in mammals and in endoparasites. In these organisms, development in a nutritive environment releases the growth constraint, but growth of cells before gastrulation requires a new program to sustain pluripotency during this growth.
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01 Nov 2005
TL;DR: The theory that biological species are descended from common ancestors provides an indispensable heuristic to understand why living organisms are what they are and do what they do.
Abstract: Nothing in biology makes sense except in the light of evolution, quipped Theodosius Dobzhansky. The theory of evolution argues that each biological species was not suddenly and independently created but that all life forms are interrelated by virtue of having descended from common ancestors through the accumulation of modifications. Indeed, nothing we know about living organisms would make any sense if they were not so interrelated. And the theory that biological species are descended from common ancestors provides an indispensable heuristic to understand why living organisms are what they are and do what they do.
974 citations
TL;DR: A monoclonal antibody is described that recognizes a conserved epitope in the homeodomain of engrailed proteins of a number of different arthropods, annelids, and chordates; this antibody is used to isolate the grasshopperEngrailed gene, a homeobox gene that has an important role in Drosophila segmentation.
582 citations
TL;DR: Progress in understanding vertebrate ZGA dynamics in frogs, fish, mice, and humans is reviewed to explore differences and emphasize common features.
262 citations
TL;DR: In Drosophila embryos, Cdk1 positive feedback serves primarily to ensure the rapid onset of mitosis, while wave propagation is regulated by S phase events, demonstrating a fundamental distinction between S phase Cdk 1 waves, which propagate as active trigger waves in an excitable medium, and mitotic Cdk2 waves, who propagate as passive phase waves.
118 citations
TL;DR: The biological and molecular characterization of cultured cells with developmental potential similar to totipotent blastomeres are reviewed, and recent progress toward the capture and stabilization of the totip powerless state in vitro is assessed.
75 citations
Cites background from "Growing an Embryo from a Single Cel..."
...The existence of a regulative state of pluripotency throughout early development can be considered an innovation of mammalian evolution (Cañon et al., 2011; O’Farrell, 2015)....
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References
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TL;DR: The Cdc2‐dependent inhibition of S phase is required in G2 for the correct ordering of the S and M phases in yeasts and Drosophila and is ascribed to its ability to phosphorylate replication factors to prevent the assembly of a preinitiation complex at the origin of replication.
Abstract: Background:
The Cdc2-dependent inhibition of S phase is required in G2 for the correct ordering of the S and M phases in yeasts and Drosophila. This function of Cdc2 has been ascribed to its ability to phosphorylate replication factors to prevent the assembly of a preinitiation complex at the origin of replication. Whether this is the sole mechanism of S phase inhibition by Cdc2 in higher metazoans is not known because the pleiotropic functions of this essential cell cycle regulator make genetic analysis difficult.
Results:
We show that Cdc2 co-expressed with Cyclin A inhibits the S phase in Drosophila salivary glands and diploid abdominal histoblasts. A kinase defective mutant of Cdc2 failed to promote mitosis, but was still able to inhibit the S phase with the same efficiency as the wild-type protein. In addition, Cdc2 and Cyclin A cooperatively inhibit transcriptional activation by the essential S phase regulator E2F. Cdc2 binds to E2F in vitro, and post-transcriptionally promotes its accumulation in vivo. Furthermore, the inhibitory effect of Cdc2 on S phase is overridden by E2F.
Conclusion:
The inhibition of S phase by Cdc2 is achieved in part by a kinase-independent mechanism, which is likely to be mediated by the inhibition of E2F.
24 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019042 5 dy of Drosophila salivary gland cells have shown that the size attained depends on ploidy (Follette et al. 1998; Hayashi and Yamaguchi 1999)....
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...dy of Drosophila salivary gland cells have shown that the size attained depends on ploidy (Follette et al. 1998; Hayashi and Yamaguchi 1999)....
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TL;DR: Comparative genomics studies reveal molecular signatures of the controversial 'phylotypic' stage — a time when embryos of members of an animal phylum all look more alike than at other embryonic stages.
Abstract: Comparative genomics studies reveal molecular signatures of the controversial 'phylotypic' stage — a time when embryos of members of an animal phylum all look more alike than at other embryonic stages. See Letters p.811 & p.815
23 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...However, the phylotypic stage occurs after important early steps in embryogenesis and the modern view considers development more like an hourglass (Raff 1996; Prud’homme and Gompel 2010)....
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TL;DR: This work examined progression through meiotic prophase I in concert with cellular mechanisms implicated in selection, growth and maturation of oocytes in this shared cytoplasm in a unique giant cell, the coenocyst.
22 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...Apparently, the nurse-cell strategy reduces the need for other adaptations to increase transcriptional output, as oocytes supported by nurse cells appear to be transcriptionally silent and to lack lampbrush chromosomes (Ganot et al. 2008)....
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TL;DR: The genome-wide distributions and temporal dynamics of nucleosomes and post-translational histone modifications through the maternal-to-zygotic transition in embryos of the pomace fly Drosophila melanogaster are described and the role of Zelda is highlighted in mediating this transition.
Abstract: A conspicuous feature of early animal development is the lack of transcription from the embryonic genome, and it typically takes several hours to several days (depending on the species) until widespread transcription of the embryonic genome begins. Although this transition is ubiquitous, relatively little is known about how the shift from a transcriptionally quiescent to transcriptionally active genome is controlled. We describe here the genome-wide distributions and temporal dynamics of nucleosomes and post-translational histone modifications through the maternal-to-zygotic transition in embryos of the pomace fly Drosophila melanogaster. At mitotic cycle 8, when few zygotic genes are being transcribed, embryonic chromatin is in a relatively simple state: there are few nucleosome free regions, undetectable levels of the histone methylation marks characteristic of mature chromatin, and low levels of histone acetylation at a relatively small number of loci. Histone acetylation increases by cycle 11, but it is not until cycle 13 that nucleosome free regions and domains of histone methylation become widespread. Early histone acetylation is strongly associated with regions that we have previously shown are bound in early embryos by the maternally deposited transcription factor Zelda. Most of these Zelda-bound regions are destined to be enhancers or promoters active during mitotic cycle 14, and our data demonstrate that they are biochemically distinct long before they become active, raising the possibility that Zelda triggers a cascade of events, including the accumulation of specific histone modifications, that plays a role in the subsequent activation of these sequences. Many of these Zelda-associated active regions occur in larger domains that we find strongly enriched for histone marks characteristic of Polycomb-mediated repression, suggesting a dynamic balance between Zelda activation and Polycomb repression. Collectively, these data paint a complex picture of a genome in transition from a quiescent to an active state, and highlight the role of Zelda in mediating this transition.
22 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...But during the early cell cycles, chromatin is relatively decompacted, repressive marks are absent, and all sequences replicate at the same time (Shermoen et al. 2010; Li et al. 2014; Yuan et al. 2014)....
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...But during the early cell cycles, chromatin is relatively decompacted, repressive marks are absent, and all sequences replicate at the same time (Shermoen et al. 2010; Li et al. 2014; Yuan et al. 2014)....
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TL;DR: It is suggested that the sorting out of nuclei into the inner mass and the outer shell of larger nuclei in middle sized oocytes is a consequence of the positions the nuclei happen to be in at the time, but that the “contest” for the role of germinal vesicle may be won by the nucleus of the outershell that has the highest ribosomal DNA content.
Abstract: The multinucleate oocytes of Flectonotus pygmaeus begin as cysts containing 2,000 or more meiotic nuclei. Each nucleus amplifies its ribosomal DNA early in oogenesis. The level of amplification is widely different from one nucleus to another, and ranges from less than 0.1 × C to more than 8 × C. The C value for this species is 1.7 × 10−12g of DNA. In oocytes of about 0.5 mm diameter the nuclei sort themselves out into an outer shell of several hundred nuclei that swell up to become much larger than the nuclei that remain in the inner compact mass. Later the outer nuclei continue to swell and decrease in number while the inner nuclei disintegrate and disappear. By the time the oocyte reaches 1.2mm diameter there are only a few large nuclei left and each has many large nucleoli and a full set of lampbrush chromosomes. Eventually, only one germinal vesicle nucleus is left, and this has all the characteristics of the single germinal vesicles that are typical of oocytes from other amphibians. It is suggested that the sorting out of nuclei into the inner mass and the outer shell of larger nuclei in middle sized oocytes is a consequence of the positions the nuclei happen to be in at the time, but that the “contest” for the role of germinal vesicle may be won by the nucleus of the outer shell that has the highest ribosomal DNA content.
21 citations