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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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Book ChapterDOI
TL;DR: The dynamics of the centrosome and its role in controlling the six stages that culminate in the cellularization of the blastoderm embryo are highlighted.
Abstract: The first 3 h of Drosophila melanogaster embryo development are exemplified by rapid nuclear divisions within a large syncytium, transforming the zygote to the cellular blastoderm after 13 successive cleavage divisions. As the syncytial embryo develops, it relies on centrosomes and cytoskeletal dynamics to transport nuclei, maintain uniform nuclear distribution throughout cleavage cycles, ensure generation of germ cells, and coordinate cellularization. For the sake of this review, we classify six early embryo stages that rely on processes coordinated by the centrosome and its regulation of the cytoskeleton. The first stage features migration of one of the female pronuclei toward the male pronucleus following maturation of the first embryonic centrosomes. Two subsequent stages distribute the nuclei first axially and then radially in the embryo. The remaining three stages involve centrosome-actin dynamics that control cortical plasma membrane morphogenesis. In this review, we highlight the dynamics of the centrosome and its role in controlling the six stages that culminate in the cellularization of the blastoderm embryo.

9 citations

Journal ArticleDOI
TL;DR: It is speculated that land plant embryogenesis has undergone three major evolutionary transformations that correspond with evolutionary transformations in the preceding ancestral phylotypic stage.
Abstract: Haeckel’s 150-year-old biogenetic law has been refuted by embryological studies of metazoans (predominantly vertebrates). However, modern empirically viable variants exist, such as the concept of the phylotypic stage that emerged predominantly from the study of metazoans. We briefly review the history of the biogenetic law and the evidence for the metazoan phylotypic stage, we explore whether a phylotypic stage exists for the land plants by comparing the embryogenesis of diploid sporophytes across nonvascular and vascular lineages, and we examine whether homologies exist for haploid gametophytes. If homology is defined as “the same structure(s) achieved by the same developmental patterning(s),” we fail to find a single phylotypic stage for land plant sporophytes or gametophytes based on morphological criteria. We speculate that land plant embryogenesis has undergone three major evolutionary transformations (heralding the appearance of bryophytes, pteridophytes, and seed plants) that correspond with evolutionary transformations in the preceding ancestral phylotypic stage.

9 citations


Cites background from "Growing an Embryo from a Single Cel..."

  • ...This stage in metazoan embryogenesis is also reached at approximately the same body size, possibly because the majority of vertebrates are oviparous or ovoviparous and because egg size varies comparatively little across animal phyla (O’Farrell 2015)....

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Journal ArticleDOI
TL;DR: The Drosophila embryo has served as an excellent model for addressing the molecular and physical mechanisms of embryonic cell cycles, with comparisons to other model systems to highlight conserved and species-specific mechanisms.
Abstract: Understanding the mechanisms of embryonic cell cycles is a central goal of developmental biology, as the regulation of the cell cycle must be closely coordinated with other events during early embryogenesis. Quantitative imaging approaches have recently begun to reveal how the cell cycle oscillator is controlled in space and time, and how it is integrated with mechanical signals to drive morphogenesis. Here, we discuss how the Drosophila embryo has served as an excellent model for addressing the molecular and physical mechanisms of embryonic cell cycles, with comparisons to other model systems to highlight conserved and species-specific mechanisms. We describe how the rapid cleavage divisions characteristic of most metazoan embryos require chemical waves and cytoplasmic flows to coordinate morphogenesis across the large expanse of the embryo. We also outline how, in the late cleavage divisions, the cell cycle is inter-regulated with the activation of gene expression to ensure a reliable maternal-to-zygotic transition. Finally, we discuss how precise transcriptional regulation of the timing of mitosis ensures that tissue morphogenesis and cell proliferation are tightly controlled during gastrulation.

7 citations

Posted ContentDOI
19 Jun 2019-bioRxiv
TL;DR: In this paper, the authors compare fixed-time sampling strategies to decisions made on-the-fly, which are based on updating and comparing the likelihoods of being at an anterior or a posterior location.
Abstract: The first cell fate decisions in the developing fly embryo are made very rapidly : hunchback genes decide in a few minutes whether a given nucleus follows the anterior or the posterior developmental blueprint by reading out the positional information encoded in the Bicoid morphogen. This developmental system constitutes a prototypical instance of the broad spectrum of regulatory decision processes that combine speed and accuracy. Traditional arguments based on fixed-time sampling of Bicoid concentration indicate that an accurate readout is not possible within the short times observed experimentally. This raises the general issue of how speed-accuracy tradeoffs are achieved. Here, we compare fixed-time sampling strategies to decisions made on-the-fly, which are based on updating and comparing the likelihoods of being at an anterior or a posterior location. We found that these more efficient schemes can complete reliable cell fate decisions even within the very short embryological timescales. We discuss the influence of promoter architectures on the mean decision time and decision error rate and present concrete promoter architectures that allow for the fast readout of the morphogen. Lastly, we formulate explicit predictions for new experiments involving Bicoid mutants.

6 citations

Journal ArticleDOI
TL;DR: In this article, the authors examined the interplay among body size, life history, and ontogeny of chelydroid turtles and found that miniaturization in the Chelydroidea clade is underlain by a dampening of the ancestral growth trajectory.
Abstract: Organismal miniaturization is defined by a reduction in body size relative to a large ancestor In vertebrate animals, miniaturization is achieved by suppressing the energetics of growth However, this might interfere with reproductive strategies in egg-laying species with limited energy budgets for embryo growth and differentiation In general, the extent to which miniaturization coincides with alterations in animal development remains obscure To address the interplay among body size, life history, and ontogeny, miniaturization in chelydroid turtles was examined The analyses corroborated that miniaturization in the Chelydroidea clade is underlain by a dampening of the ancestral growth trajectory There were no associated shifts in the early sequence of developmental transformations, though the relative duration of organogenesis was shortened in miniaturized embryos The size of eggs, hatchlings, and adults was positively correlated within Chelydroidea A phylogenetically broader exploration revealed an alternative miniaturization mode wherein exceptionally large hatchlings grow minimally and thus attain diminutive adult sizes Lastly, it is shown that miniaturized Chelydroidea turtles undergo accelerated ossification coupled with a ~10% reduction in shell bones As in other vertebrates, the effects of miniaturization were not systemic, possibly owing to opposing functional demands and tissue geometric constraints This underscores the integrated and hierarchical nature of developmental systems

5 citations

References
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Journal ArticleDOI
25 Aug 2006-Cell
TL;DR: Induction of pluripotent stem cells from mouse embryonic or adult fibroblasts by introducing four factors, Oct3/4, Sox2, c-Myc, and Klf4, under ES cell culture conditions is demonstrated and iPS cells, designated iPS, exhibit the morphology and growth properties of ES cells and express ES cell marker genes.

23,959 citations


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

  • ...Tremendous advances in the study of stem cells have identified mammalian factors that can reprogram differentiated cells to pluripotency (Takahashi and Yamanaka 2006)....

    [...]

Journal ArticleDOI
09 Jul 1981-Nature
TL;DR: The establishment in tissue culture of pluripotent cell lines which have been isolated directly from in vitro cultures of mouse blastocysts are reported, able to differentiate either in vitro or after innoculation into a mouse as a tumour in vivo.
Abstract: Pluripotential cells are present in a mouse embryo until at least an early post-implantation stage, as shown by their ability to take part hi the formation of chimaeric animals1 and to form teratocarcinomas2. Until now it has not been possible to establish progressively growing cultures of these cells in vitro, and cell lines have only been obtained after teratocarcinoma formation in vivo. We report here the establishment in tissue culture of pluripotent cell lines which have been isolated directly from in vitro cultures of mouse blastocysts. These cells are able to differentiate either in vitro or after innoculation into a mouse as a tumour in vivo. They have a normal karyotype.

8,144 citations

Journal ArticleDOI
TL;DR: In this article, the authors described the establishment directly from normal preimplantation mouse embryos of a cell line that forms teratocarcinomas when injected into mice and demonstrated the pluripotency of these embryonic stem cells by the observation that subclonal cultures, derived from isolated single cells, can differentiate into a wide variety of cell types.
Abstract: This report describes the establishment directly from normal preimplantation mouse embryos of a cell line that forms teratocarcinomas when injected into mice. The pluripotency of these embryonic stem cells was demonstrated conclusively by the observation that subclonal cultures, derived from isolated single cells, can differentiate into a wide variety of cell types. Such embryonic stem cells were isolated from inner cell masses of late blastocysts cultured in medium conditioned by an established teratocarcinoma stem cell line. This suggests that such conditioned medium might contain a growth factor that stimulates the proliferation or inhibits the differentiation of normal pluripotent embryonic cells, or both. This method of obtaining embryonic stem cells makes feasible the isolation of pluripotent cells lines from various types of noninbred embryo, including those carrying mutant genes. The availability of such cell lines should made possible new approaches to the study of early mammalian development.

5,496 citations

Journal ArticleDOI
TL;DR: The Copernican world model has been shown to be a "mere theory" as mentioned in this paper, not a "fact," and it has not been verified by direct observations even to the extent the sphericity of the earth has been observed.
Abstract: As RECENTLY AS 1966, sheik Abd el Aziz bin Baz asked the king of Saudi Arabia to suppress a heresy that was spreading in his land. Wrote the sheik: "The Holy Koran, the Prophet's teachings, the majority of Islamic scientists, and the actual facts all prove that the sun is running in its orbit ... and that the earth is fixed and stable, spread out by God for his mankind. ... Anyone who professed otherwise would utter a charge of falsehood toward God, the Koran, and the Prophet." 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 had 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. Parts of the Copernican world model, such as the contention that the earth rotates around the sun, and not vice versa, have not been verified by direct observations even to the extent the sphericity of the earth has been. Yet scientists accept the model as an accurate representation of reality. Why? Because it makes sense of a multitude of facts which are otherwise meaningless or extravagant. To nonspecialists most of these facts are unfamiliar. Why then do we accept the "mere theory" that the earth is a sphere revolving around a spherical sun? Are we simply submitting to authority? Not quite: we know that those who took time to study the evidence found it convincing. The good sheik is probably ignorant of the evidence. Even more likely, he is so hopelessly biased that no amount of evidence would impress him. Anyway, it would be sheer waste of time to attempt to convince him. The Koran and the Bible do not contradict Copernicus, nor does Copernicus contradict them. It is ludicrous to mistake the Bible and the Koran for primers of natural science. They treat of matters even more important: the meaning of man and his relations to God. They are written in poetic symbols that were understandable to people of the age when they were written, as well as to peoples of all other ages. The king of Arabia did not comply with the sheik's demand. He knew that some people fear enlightenment, because enlightenment threatens their vested interests. Education is not to be used to promote obscurantism. The earth is not the geometric center of the universe, although it may be its spiritual center. It is a mere speck of dust in cosmic spaces. Contrary to Bishop Ussher's calculations, the world did not appear in approximately its present state in 4004 B.C. The estimates of the age of the universe given by modern cosmologists are still only rough approximations, which are revised (usually upward) as the methods of estimation are refined. Some cosmologists take the universe to be about 10 billion years old; others suppose that it may have existed, and will continue to exist, eternally. The origin of life on earth is dated tentatively between 3 and 5 billion years ago; manlike beings appeared relatively quite recently, between 2 and 4 million years ago. The estimates of the age of the earth, of the duration of the geologic and paleontologic eras, and of the antiquity of man's ancestors are now based mainly on radiometric evidence-the proportions of isotopes of certain chemical elements in rocks suitable for such studies.

2,143 citations

Journal ArticleDOI
01 Oct 1982-Cell
TL;DR: The Xenopus embryo undergoes 12 rapid synchronous cleavages followed by a period of slower asynchronous divisions more typical of somatic cells, termed the midblastula transition (MBT), which shows that at the MBT the blastomeres become motile and transcriptionally active for the first time.

1,587 citations