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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: A general relationship between metabolic rate and incubation time is obtained; namely in different species of birds that have the same egg weight the natural incubation period is inversely related to the metabolic rate or the egg shell gas conductance.

215 citations


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

  • ...The relationship between developmental time and growth is perhaps most obvious in birds, in which the time to hatching in different species increases in proportion to the size of the egg and the hatchling it eventually produces (Rahn et al. 1974)....

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Journal ArticleDOI
30 Aug 2013-Science
TL;DR: It is found that zebrafish Pou5f1, a homolog of the mammalian pluripotency transcription factor Oct4, occupies SOX-POU binding sites before the onset of zygotic transcription and activates the earliestZygotic genes.
Abstract: The development of multicellular animals is initially controlled by maternal gene products deposited in the oocyte. During the maternal-to-zygotic transition, transcription of zygotic genes commences, and developmental control starts to be regulated by zygotic gene products. In Drosophila, the transcription factor Zelda specifically binds to promoters of the earliest zygotic genes and primes them for activation. It is unknown whether a similar regulation exists in other animals. We found that zebrafish Pou5f1, a homolog of the mammalian pluripotency transcription factor Oct4, occupies SOX-POU binding sites before the onset of zygotic transcription and activates the earliest zygotic genes. Our data position Pou5f1 and SOX-POU sites at the center of the zygotic gene activation network of vertebrates and provide a link between zygotic gene activation and pluripotency control.

212 citations


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

  • ...These factors appear to act widely to direct transcription of genes necessary to stimulate the developmental potential of the blastomeres of the zebrafish embryo (Lee et al. 2013; Leichsenring et al. 2013)....

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Journal ArticleDOI
TL;DR: It is demonstrated that bucky ball functions during early oogenesis to regulate polarity of the oocyte, future egg and embryo, and the expansion of animal identity in oocytes and somatic follicle cells suggests that somatic cell fate and oocyte polarity are interdependent.

209 citations

Journal ArticleDOI
TL;DR: It is proposed that comparison to the rapid peri-gastrulation cycles is more appropriate and suggested that these cycles are related by evolutionary descent to the early cleavage stages of embryos such as those of frog and fly.

204 citations


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

  • ...To a large extent, it is the nonyolky cytoplasm that undergoes this phase 2 program to produce an elemental phylotypic embryo, and later the yolk is called on to fund a third phase in the growth and proliferation program, the expansion phase (O’Farrell 2004, 2011; O’Farrell et al. 2004)....

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  • ...In addition to being fast, other similarities that I have previously reviewed suggest parallels between these pregastrulation cell cycles in mammals and the early cleavage cycles (O’Farrell et al. 2004)....

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  • ...If, instead, we align development at the phylotypic stage (O’Farrell et al. 2004), one is struck by the close relationships among the embryos of these model vertebrate organisms, as was von Baer two centuries ago....

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  • ...This insertion obscures relationships even with close vertebrate relatives (O’Farrell et al. 2004)....

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  • ...Understanding the specializations of mammalian development in this context can be illuminating (O’Farrell et al. 2004)....

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Journal ArticleDOI
14 Oct 2014-eLife
TL;DR: Early histone acetylation is strongly associated with regions that have been shown to be bound in early embryos by the maternally deposited transcription factor Zelda, suggesting 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.
Abstract: We describe the genome-wide distributions and temporal dynamics of nucleosomes and post-translational histone modifications throughout the maternal-to-zygotic transition in embryos of 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 12, but it is not until cycle 14 that nucleosome free regions and domains of histone methylation become widespread. Early histone acetylation is strongly associated with regions that we have previously shown to be bound in early embryos by the maternally deposited transcription factor Zelda, suggesting 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.

193 citations