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Journal ArticleDOI

Growing an Embryo from a Single Cell: A Hurdle in Animal Life

01 Nov 2015-Cold Spring Harbor Perspectives in Biology (Cold Spring Harbor Lab)-Vol. 7, Iss: 11
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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Citations
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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

Journal ArticleDOI
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

Journal ArticleDOI
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

Journal ArticleDOI
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

Journal ArticleDOI
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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Journal ArticleDOI
TL;DR: The results of this ultrastructural study lend support to the hypothesis that the germinal cells of digeneans are germ line cells.
Abstract: The germinal mass in Himasthla elongata rediae was studied in detail using transmission electron microscopy. It was shown to be a specialized reproductive organ consisting of germinal cells at various maturation stages, supporting cells and stem cells. The germinal mass also contains early cercarial embryos emerging as a result of cleavage division of mature germinal cells. The stem cells that give rise to germinal cells have heterochromatin-rich nuclei with distinct nucleoli and scarce cytoplasm containing mainly free ribosomes and few mitochondria. The differentiating germinal cells undergo a growth, which is accompanied by an emergence of annulate lamellae and the nuage in their cytoplasm, a noticeable development of RER and Golgi apparatus and an increase in the number of mitochondria. The mitochondria form a large group at one of the cell poles. During differentiation, the nucleus and nucleolus of the germinal cell enlarge while the chromatin becomes gradually less condensed. The supporting tissue of the germinal mass is made up of cells connected by septate junctions. These supporting cells are distinctly different in cellular shape and nuclear ultrastructure. Their outgrowths form a tight meshwork housing stem cells, germinal cells and early cercarial embryos. The cytoplasm of the supporting cells in the mesh area is separated into fine parallel layers by labyrinthine narrow cavities communicating with the intercellular space. The supporting tissue contains differentiating and degenerating cells which indicates its renewal. The results of this ultrastructural study lend support to the hypothesis that the germinal cells of digeneans are germ line cells.

12 citations

Journal ArticleDOI
TL;DR: Lampbrush chromosomes are transcriptionally active chromosomes found in the germinal vesicle of large oocytes of many vertebrate and invertebrate animals and also in the giant single-celled alga Acetabularia, and provide unique opportunities to study reprogramming at the level of the individual transcription unit.
Abstract: Lampbrush chromosomes (LBCs) are transcriptionally active chromosomes found in the germinal vesicle (GV) of large oocytes of many vertebrate and invertebrate animals and also in the giant single-celled alga Acetabularia These cells are all in prophase of the first meiotic division Nevertheless, many meiotic cells do not develop LBCs, arguing that LBCs are not an essential feature of meiosis LBCs probably represent the most active transcriptional state that can be attained by cells that must give rise to diploid progeny Polyploidy permits cells to reach higher rates of transcription per nucleus but precludes a return to diploidy In this sense, LBCs represent a relatively inefficient transcriptional compromise employed by large meiotic cells These considerations help to explain why transcriptionally active GVs develop LBCs, but they do not explain why LBCs have never been seen in somatic cells, diploid or otherwise If LBCs are truly limited to germ cells, then some of their unusual features may reflect reprogramming of the genome If this is the case, LBCs provide unique opportunities to study reprogramming at the level of the individual transcription unit

11 citations


"Growing an Embryo from a Single Cel..." refers background in this paper

  • ...This stage often persists for months as the oocyte enlarges, and studies in Xenopus showed that oocyte transcripts accumulate during this period (Gall 2012; Kloc et al. 2014)....

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Journal Article
TL;DR: The oocyte nuclei of these beetles are characterized by the absence of RNA synthesizing nucleolar system and, as compared with the trophocytes, by the low level of RNA synthesis on the chromosomes.
Abstract: Changes in the nuclear structures and their participation in RNA synthesis in the growing oocytes were followed in two species of beetles Blaps lethifera and Gnaptor spinimanus. In the oocytes of both the species, the chromosomes join into the karyosphere following the short-term lampbrush stage. A large capsule appears around the karayosphere which consists of the fibrous substance, granules and karyosphere nucleoli. The latter form in the karyosphere and contain RNP but they are not true nucleoli since they do not include 3H-uridine. RNA synthesis on the chromosomes, active at the lampbrush stage, falls markedly following their joining into the karyosphere. The oocyte nuclei of these beetles are, thus, characterized by the absence of RNA synthesizing nucleolar system and, as compared with the trophocytes, by the low level of RNA synthesis on the chromosomes.

10 citations


"Growing an Embryo from a Single Cel..." refers background in this paper

  • ...For example, lampbrush chromosomes have been described in organisms representing mollusks, arthropods, echinoderms and chordates (Bedford, 1966; Gall et al., 2004; Gruzova and Batalova, 1979; Smiley, 1990)....

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Journal ArticleDOI
TL;DR: Development of spines was observed in juvenile and mature adult worms, and morphological features of the adult worm observed for the first time in a Brachylaima were the unarmed cirrus extended from the genital pore with released sperm present and the Laurer's canal opening visible in tegumental folds on the dorsal surface.
Abstract: Brachylaima cribbi is a recently described species of terrestrial trematode that infects mammals and birds with helicid land snails as its first and second intermediate hosts. The adult worm is 2.5‐ 6.0 mm long by 0.5 ‐0.8 mm wide being a long slender cylindrical worm with oral and ventral suckers in the anterior quarter and genital pore in the posterior quarter. Scanning electron microscopy shows that there is a dense covering of tegumental spines at the anterior end which diminishes towards the posterior extremities of the worm. Development of spines was observed in juvenile and mature adult worms. In young worms 1 ‐3 weeks post infection (wpi) spines appear as buds with a serrated edge each having 1‐ 4 spikes per spine. As the worm ages the spines broaden and by 5 wpi the number of spikes per spine increases to an average of 8.1. The serial development of oral sucker papillae in the cercaria, metacercaria and adult worm was observed with the finding of an elongated papilla with a bifurcated tip on the cercaria becoming a shorter and thicker elongated papilla with a large central stoma on the metacercaria. In the adult worm, this papilla becomes dome-shaped with a small central stoma. For some of these papillae a cilium could be seen extended from the central stoma. Other life-cycle stages illustrated were the hatched egg with an extruded egg membrane minus an operculum and a portion of the branched sporocyst dissected from the digestive gland of the land snail Theba pisana showing a terminal birth pore. Scanning electron microscopy morphological features of the adult worm observed for the first time in a Brachylaima were the unarmed cirrus extended from the genital pore with released sperm present and the Laurer’s canal opening visible in tegumental folds on the dorsal surface approximately 300mm posterior to the genital pore.

9 citations


"Growing an Embryo from a Single Cel..." refers background in this paper

  • ...The parasites, often hermaphroditic, produce small encysted eggs that are released from the infected primary host (Butcher et al. 2002)....

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Journal ArticleDOI
TL;DR: The hypothesis that mammalian blastocyst regulatory networks evolved through rewiring of pre-existing components, involving the co-option and duplication of existing genes and the establishment of new regulatory interactions among them, is strongly supported.
Abstract: Early mammalian development is characterized by a highly specific stage, the blastocyst, by which embryonic and extraembryonic lineages have been determined, but pattern formation has not yet begun. The blastocyst is also of interest because cell precursors of the embryo proper retain for a certain time the capability to generate all the cell types of the adult animal. This embryonic pluripotency is established and maintained by a regulatory network under the control of a small set of transcription factors, comprising Oct4, Sox2 and Nanog. This network is largely conserved in eutherian mammals, but there is scarce information about how it arose in vertebrates. We have analysed the conservation of gene regulatory networks controlling blastocyst lineages and pluripotency in the mouse by comparison with the chick. We found that few of elements of the network are novel to mammals; rather, most of them were present before the separation of the mammalian lineage from other amniotes, but acquired novel expressio...

5 citations


"Growing an Embryo from a Single Cel..." refers background in this paper

  • ...As discussed below, even though these mechanisms are set in a different context in mammalian development, an understanding of the ancestral mechanism will give us deeper insight into this process in mammals (Cañon et al. 2011; Sánchez-Sánchez et al. 2011; Marandel et al. 2012; Lee et al. 2013)....

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  • ...As discussed below, even though these mechanisms are set in a different context in mammalian development, an understanding of the ancestral mechanism will give us deeper insight into this process in mammals (Cañon et al. 2011; Sánchez-Sánchez et al. 2011; Marandel et al. 2012; Lee et al. 2013)....

    [...]