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 anatomy and fine structure of the echinoderm ovary is described, with emphasis on both the cellular relationships of the germ line cells to the somatic cells of the inner epithelium, and on the neuromuscular systems.
Abstract: This review of the anatomical, histological, biochemical, and molecular biological literature on echinoderm oogenesis includes the entire developmental history of oocytes; from their inception to the time they become ova. This is done from a comparative perspective, with reference to members of the five extant echinoderm classes; crinoids, holothurians, asteroids, ophiuroids, and echinoids. I describe the anatomy and fine structure of the echinoderm ovary, with emphasis on both the cellular relationships of the germ line cells to the somatic cells of the inner epithelium, and on the neuromuscular systems. I review the literature on the growth of oogonia into fully formed oocytes, including the process of vitellogenesis, presenting an ultrastructural analysis of the organelles and extracellular structures found in fully formed echinoderm oocytes. Echinoderm oocyte maturation is reviewed and a description of the ultrastructural, biochemical and molecular biological changes thought to occur during this process is presented. Finally, I discuss oocyte ovulation, the severing of cellular connections between the oocyte and its surrounding somatic epithelial cells.
49 citations
"Growing an Embryo from a Single Cel..." refers background or result in this paper
...…of autonomous oocyte growth in sampled species of various other animal phyla, including chordates, echinoderms, mollusks, and cnidarians, and a group of more primitive animals, such as jellyfish (Smiley 1990; Eckelbarger and Larson 1992; Eckelbarger and Young 1997; Marlow and Mullins 2008)....
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...Given the limitation imposed by the transcriptional potency of a single nucleus, how does autonomous growth succeed at producing oocytes? To a large degree, the answer is that oocytes using this program grow much more slowly, generally taking several months to more than a year to reach a mature size (Smiley 1990)....
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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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...To a large degree, the answer is that oocytes using this program grow much more slowly, generally taking several months to more than a year to reach a mature size (Smiley 1990)....
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...This interpretation is consistent with findings of autonomous oocyte growth in sampled species of various other animal phyla, including chordates, echinoderms, mollusks, and cnidarians, and a group of more primitive animals, such as jellyfish (Smiley 1990; Eckelbarger and Larson 1992; Eckelbarger and Young 1997; Marlow and Mullins 2008)....
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TL;DR: Yemanuclein (YEM), the Drosophila member of the Hpc2/Ubinuclein family, is essential for histone deposition in the male pronucleus and the alternative ATRX/XNP-dependent H3.3 deposition pathway is shown to be not involved in paternal chromatin assembly, underlining the specific implication of the HIRA/YEM complex for this essential step of zygote formation.
Abstract: The differentiation of post-meiotic spermatids in animals is characterized by a unique reorganization of their nuclear architecture and chromatin composition. In many species, the formation of sperm nuclei involves the massive replacement of nucleosomes with protamines, followed by a phase of extreme nuclear compaction. At fertilization, the reconstitution of a nucleosome-based paternal chromatin after the removal of protamines requires the deposition of maternally provided histones before the first round of DNA replication. This process exclusively uses the histone H3 variant H3.3 and constitutes a unique case of genome-wide replication-independent (RI) de novo chromatin assembly. We had previously shown that the histone H3.3 chaperone HIRA plays a central role for paternal chromatin assembly in Drosophila. Although several conserved HIRA-interacting proteins have been identified from yeast to human, their conservation in Drosophila, as well as their actual implication in this highly peculiar RI nucleosome assembly process, is an open question. Here, we show that Yemanuclein (YEM), the Drosophila member of the Hpc2/Ubinuclein family, is essential for histone deposition in the male pronucleus. yem loss of function alleles affect male pronucleus formation in a way remarkably similar to Hira mutants and abolish RI paternal chromatin assembly. In addition, we demonstrate that HIRA and YEM proteins interact and are mutually dependent for their targeting to the decondensing male pronucleus. Finally, we show that the alternative ATRX/XNP-dependent H3.3 deposition pathway is not involved in paternal chromatin assembly, thus underlining the specific implication of the HIRA/YEM complex for this essential step of zygote formation.
48 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...Hira is a conserved member of a protein complex that acts as an H3/H4 chaperone to promote replication-independent deposition of nucleosomes (Orsi et al. 2013)....
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TL;DR: It is concluded that the enormous complement of oocytes mitochondria is accumulated well before the end of oocyte growth and is maintained at a constant level during the remainder of oogenesis, through maturation, fertilization, and on into early development.
46 citations
TL;DR: The aim of this review is to consider why this translational control phase exists and how translationalcontrol operates during this early phase of maturation, and to consider aspects of translational Control that occur in adult somatic ceils.
Abstract: The giant unicellular alga, Acetabularia, can develop a complex f ru i t i ng body in the absence of a nucleus (H~immerling~ 1963), a process which can be regulated wholly by translational control (Harr is , 1968; Brachet~ 1968). Exactly analogous independence of nuclear act ivi ty is found in the development of animals. Take the frog's egg as an example. In the ovary the oocyte is stimulated by progesterone to complete meiosis, thus becoming an egg, and to be ovulated. As we shall see, this process of maturation involves changes in protein synthesisr ye t it can happen when RNA synthesis is prevented with inhibitors or by enucleation (Smith & EckeG 1969a; Merriam, 1972; Bal tus e t al., 1973; Schorderet-Slatkine, I972; Shorderet-Slatkine & Drury, 1973; Adamson & Woodland, 1977). Once laid and fertilized, the egg ~may be injected with actinomycin D to block RNA synthesis, but development is apparently normal up to gastrulation~ though not beyond (Brache t & Denis, 1963; Brachet et a l , 1964; Wallace & Elsdale, 1963). In the frog, Xenopus, about 30 000 cells are produced without the intervention of the genome. All other early embryos examined show similar independence of transcription (review by Davidson, 1976). This includes even mammalian embryos; the mouse can develop without RNA synthesis for the first 27 h of development9 although it has reached only the two-cell stage by this time (review by 3ohnson, 1981). The aim of this review is to consider why this translational control phase exists and how translational control operates during this early phase of d e v e l o p m e n t . I shall not consider aspects of translational control that occur in adult somatic ceils.
41 citations
"Growing an Embryo from a Single Cel..." refers background in this paper
...As pointed out by Woodland (1982), the rate at which a gene can produce transcripts is limited, and this limitation imposes practical limitations on the growth and function of large cells....
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...Slow accumulation of transcripts would stymie the progress of development (Woodland 1982)....
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TL;DR: The good sheik evidently holds the Copernican theory to be a "mere theory," not a "fact," and in this he is technically correct.
Abstract: The good sheik evidently holds the Copernican theory to be a \"mere theory,\" not a \"fact.\" In this he is technically correct. A theory can be verified by a mass of facts, but it becomes a proven theory, not a fact. The sheik was perhaps unaware that the Space Age had begun before he asked the king to suppress the Copernican heresy. The sphericity of the earth has been seen by astronauts, and even by many earth-bound people on their television screens. Perhaps the sheik could retort that those who venture beyond the confines of God’s earth suffer hallucinations, and that the earth is really flat.
37 citations