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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 differing biological purposes of quyingcence, and the coupling of quiescence in metazoans to growth and to the structuring of tissues during development are described.
Abstract: Cell cycle investigations have focused on relentless exponential proliferation of cells, an unsustainable situation in nature. Proliferation of cells, whether microbial or metazoan, is interrupted by periods of quiescence. The vast majority of cells in an adult metazoan lie quiescent. As disruptions in this quiescence are at the foundation of cancer, it will be important for the field to turn its attention to the mechanisms regulating quiescence. While often presented as a single topic, there are multiple forms of quiescence each with complex inputs, some of which are tied to conceptually challenging aspects of metazoan regulation such as size control. In an effort to expose the enormity of the challenge, I describe the differing biological purposes of quiescence, and the coupling of quiescence in metazoans to growth and to the structuring of tissues during development. I emphasize studies in the organism rather than in tissue culture, because these expose the diversity of regulation. While quiescence is likely to be a primitive biological process, it appears that in adapting quiescence to its many distinct biological settings, evolution has diversified it. Consideration of quiescence in different models gives us an overview of this diversity.

68 citations


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

  • ...The subsequent phases of growth were described in previous reviews (O’Farrell 2004, 2011; O’Farrell et al. 2004)....

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  • ...The central features of growth in phases 3 and 4 were described in two previous reviews (O’Farrell 2004, 2011)....

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  • ...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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Journal ArticleDOI
TL;DR: It is demonstrated that the Dub3 gene is a direct target of Esrrb, a key transcription factor of the self-renewal machinery, and its expression is strongly downregulated during neural conversion and precedes Cdc25A destabilization, while forced Dub3 expression in ESCs becomes lethal upon differentiation.

59 citations

Journal ArticleDOI
TL;DR: Development of a method of infecting of the molluscan host by microsurgical transplantation of the parasite's sporocysts enables the researcher to maintain the host cycle of Schistosoma mansoni exclusively by asexual means and without the participation of a vertebrate host.

55 citations

Journal ArticleDOI
01 Jan 1996-Genetics
TL;DR: To the cytoplasm of the sea urchin egg only the initial and simplest properties responsible for differentiation are ascribed, the most general basic form, the framework within which all specific details are filled in by the nucleus.
Abstract: It appears that the initial steps up to the [sea urchin] blastula stage are independent of the quality of the nuclear substance, even though it is essential that the nuclear substance be of a kind capable of existing in the egg. The necessity for particular chromosomes becomes apparent first with the formation of the primary mesenchyme and from then on shows up in all processes as far as development can be observed. . . . With respect to those characters in which we are able to recognize individual variations, the nuclear substance and not the cyte plasmic cell substance imposes its specific character on the developing trait. . . . Earlier stages, for which according to our results, specific chromosomes are not necessary, demonstrate a purely maternal character. . . . I would like to ascribe to the cytoplasm of the sea urchin egg only the initial and simplest properties responsible for differentiation. . . it provides the most general basic form, the framework within which all specific details are filled in by the nucleus.

54 citations


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

  • ...In part, this is a progressive transition with additional zygotic functions coming into play as persisting maternal functions are successively eliminated (Wieschaus 1996; Follette and O’Farrell 1997)....

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Journal ArticleDOI
TL;DR: Examination of related species indicated that the coenocyst arrangement is a conserved feature of Appendicularian oogenesis allowing efficient numerical adjustment of oocyte production, clearly a common and successful reproductive strategy on a global scale.

54 citations


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

  • ...Nurse cells are also used in annelids, and a related nurse-cell type of oogenesis has been discovered in a group of chordate species whose lifestyle relies on rapid oogenesis (Ganot et al. 2007)....

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