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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 slowing of S phase is an active process, not a titration of maternal replication machinery, but increasing delays in the replication of satellite sequences extend S phase.

111 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 chromatin do appear, they do so in a sequence as if heterochromatin formation is an integral part of the developmental program (Shermoen et al. 2010)....

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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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  • ...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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  • ...Additionally, heterochromatic DNA replicates later than euchromatic sequences, and the sequential replication of different regions of the genome is the main reasons that S phase is normally long (Shermoen et al. 2010)....

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  • ...chromatin do appear, they do so in a sequence as if heterochromatin formation is an integral part of the developmental program (Shermoen et al. 2010)....

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Journal ArticleDOI
TL;DR: The results indicate that the gonad is the primary site of mtDNA replication, whilst the mtDNA of adult somatic tissues mainly stems from the developing embryo, and it is shown that the mt DNA copy number shows great plasticity as it can be almost tripled as a response to the environmental stimuli.
Abstract: A number of studies showed that the development and the lifespan of Caenorhabditis elegans is dependent on mitochondrial function. In this study, we addressed the role of mitochondrial DNA levels and mtDNA maintenance in development of C. elegans by analyzing deletion mutants for mitochondrial polymerase gamma (polg-1(ok1548)). Surprisingly, even though previous studies in other model organisms showed necessity of polymerase gamma for embryonic development, homozygous polg-1(ok1548) mutants had normal development and reached adulthood without any morphological defects. However, polg-1 deficient animals have a seriously compromised gonadal function as a result of severe mitochondrial depletion, leading to sterility and shortened lifespan. Our results indicate that the gonad is the primary site of mtDNA replication, whilst the mtDNA of adult somatic tissues mainly stems from the developing embryo. Furthermore, we show that the mtDNA copy number shows great plasticity as it can be almost tripled as a response to the environmental stimuli. Finally, we show that the mtDNA copy number is an essential limiting factor for the worm development and therefore, a number of mechanisms set to maintain mtDNA levels exist, ensuring a normal development of C. elegans even in the absence of the mitochondrial replicase.

103 citations


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

  • ...Additionally, a mutant lacking the late increase in mitochondrial genomes produces mature adults (Tsang and Lemire 2002; Bratic et al. 2009)....

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Journal ArticleDOI
TL;DR: The low rate of RNA synthesis found in eggs, but not in oocytes, is therefore not caused by simple precursor control and may be correlated with the ability of eggs to induce nuclear DNA synthesis, a property not shown by oocytes.
Abstract: The ribonucleotide and deoxyribonucleotide contents of eggs and oocytes of Xenopus laevis were measured. Eggs contained most deoxyribonucleotide in the form of triphosphates. dCTP, dTTP, dATP and dGTP were present in similar amounts. The egg contained sufficient deoxynucleotide triphosphate to make approximately 2500 nuclei. Oocytes contained less pyrimidine deoxyribonucleoside triphosphates than did eggs, and purine deoxyribonucleoside triphosphates were not detected. These differences may be correlated with the ability of eggs to induce nuclear DNA synthesis, a property not shown by oocytes. Both oocytes and eggs seem to contain non-phosphorylated, α-unsubstituted aldehydes, which may be deoxyribose derivatives. Eggs and oocytes contain similar amounts of ribonucleoside triphosphates. The low rate of RNA synthesis found in eggs, but not in oocytes, is therefore not caused by simple precursor control.

95 citations

Journal ArticleDOI
01 Oct 2012-Evodevo
TL;DR: While the evolution of amniotes was believed to have involved the loss of gills and their covering, the operculum, it is now apparent that neither of these structures was completely lost and the key steps in the phylogenetic history are laid out during the development of the pharyngeal apparatus.
Abstract: The vertebrate pharyngeal apparatus, serving the dual functions of feeding and respiration, has its embryonic origin in a series of bulges found on the lateral surface of the head, the pharyngeal arches. Developmental studies have been able to discern how these structures are constructed and this has opened the way for an analysis of how the pharyngeal apparatus was assembled and modified during evolution. For many years, the role of the neural crest in organizing pharyngeal development was emphasized and, as this was believed to be a uniquely vertebrate cell type, it was suggested that the development of the pharyngeal apparatus of vertebrates was distinct from that of other chordates. However, it has now been established that a key event in vertebrate pharyngeal development is the outpocketing of the endoderm to form the pharyngeal pouches. Significantly, outpocketing of the pharyngeal endoderm is a basal deuterostome character and the regulatory network that mediates this process is conserved. Thus, the framework around which the vertebrate pharyngeal apparatus is built is ancient. The pharyngeal arches of vertebrates are, however, more complex and this can be ascribed to these structures being populated by neural crest cells, which form the skeletal support of the pharynx, and mesoderm, which will give rise to the musculature and the arch arteries. Within the vertebrates, as development progresses beyond the phylotypic stage, the pharyngeal apparatus has also been extensively remodelled and this has seemingly involved radical alterations to the developmental programme. Recent studies, however, have shown that these alterations were not as dramatic as previously believed. Thus, while the evolution of amniotes was believed to have involved the loss of gills and their covering, the operculum, it is now apparent that neither of these structures was completely lost. Rather, the gills were transformed into the parathyroid glands and the operculum still exists as an embryonic entity and is still required for the internalization of the posterior pharyngeal arches. Thus, the key steps in our phylogenetic history are laid out during the development of our pharyngeal apparatus.

80 citations


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

  • ...…taken by some as evidence for a claim that ontogeny recapitulates phylogeny—or that the developmental sequence passes through all of the evolutionary steps as if “more advanced” organisms achieve their distinctions by late additions to the developmental sequence (e.g., Graham and Richardson 2012)....

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Journal ArticleDOI
TL;DR: The germinal vesicle of Xenopus laevis is an enormous nucleus that contains 18 giant lampbrush chromosomes and thousands of inclusions, which make the GV an ideal object for analysis of nuclear structure and function.

80 citations


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

  • ...Avariety of specialized structures have been described in the germinal vesicle (Gall et al. 2004; Gardner et al. 2012)....

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

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  • ...As expected, when growth is autonomous, the oocyte nucleus is transcriptionally active (Gall et al. 2004)....

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