Growing an Embryo from a Single Cell: A Hurdle in Animal Life

doi:10.1101/CSHPERSPECT.A019042

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Growing an Embryo from a Single Cell: A Hurdle in Animal Life

Journal Article•DOI•

Growing an Embryo from a Single Cell: A Hurdle in Animal Life

Patrick H. O'Farrell¹•Institutions (1)

University of California, San Francisco¹

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.

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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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Nothing in Biology Makes Sense Except in the Light of Evolution

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Raghavendra Gadagkar

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.

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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.

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974 citations

Journal Article•DOI•

Expression of engrailed proteins in arthropods, annelids and chordates

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N.H. Patel

01 Jan 1989-Trends in Genetics

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.

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582 citations

Journal Article•DOI•

Zygotic Genome Activation in Vertebrates.

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David Jukam¹, S. Ali M. Shariati¹, Jan M. Skotheim¹•Institutions (1)

Stanford University¹

21 Aug 2017-Developmental Cell

TL;DR: Progress in understanding vertebrate ZGA dynamics in frogs, fish, mice, and humans is reviewed to explore differences and emphasize common features.

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262 citations

Journal Article•DOI•

Waves of Cdk1 Activity in S Phase Synchronize the Cell Cycle in Drosophila Embryos

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Victoria E. Deneke¹, Anna Melbinger², Massimo Vergassola², Stefano Di Talia¹•Institutions (2)

Duke University¹, University of California, San Diego²

22 Aug 2016-Developmental Cell

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.

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118 citations

Journal Article•DOI•

Capturing Totipotent Stem Cells

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Christopher L. Baker, Martin F. Pera

04 Jan 2018-Cell Stem Cell

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.

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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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Journal Article•DOI•

Illuminating DNA replication during Drosophila development using TALE-lights

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Kai Yuan¹, Antony W. Shermoen¹, Patrick H. O'Farrell¹•Institutions (1)

University of California, San Francisco¹

17 Feb 2014-Current Biology

TL;DR: It is shown that the compact foci of satellite sequences expand in conjunction with their replication and that a satellite sequence shows a particularly marked shift to later replication in the cell cycle after the midblastula transition (MBT), which suggests that developmental signals can separately influence the timing of different satellite sequences.

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37 citations

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

...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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Journal Article•DOI•

Multiple nuclei during early oogenesis in flectonotus pygmaeus and other marsupial frogs

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Eugenia M. del Pino, A. A. Humphries

01 Apr 1978-The Biological Bulletin

TL;DR: The occurrence of niultinucleate stages as a regular feature of oogenesis in several genera of marsupial frogs of South America is reported.

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Abstract: In the great majority of amphibians yet investigated the occurrence of oocytes with more than one nucleus or more than a single liieiotiC figure is exceptional (Humphries, 1956,1966 ; Parnienter, Derezin andParnienter, 1960 ; Humphrey, 1963) . In the tailed frog Asca/'hus (mel, however, Macgregor and Kezer ( 1970) found that oogenesis regularly involves oocytes with eight nuclei, all but one of @yhich disappear before the final stages of oogenesis. When a related species, Leiopelnta hochstetteri, was investigated by Robinson, Stephenson and Stephenson ( 1973) , onlya single binucleate oocyte wasfoundamong 26oocytes examined. In the present paper the occurrence of niultinucleate stages as a regular feature of oogenesis in several genera of marsupial frogs of South America is reported. The multinucleate condition is associated with the early stages of oogenesis; in large, yolky oocytes only one nucleus is present. Most of the marsupial frogs are inhabitants of the humid forests of South America. In these frogs the aquatic larval stages are reduced or eliminated al together, a phenomenon associated with the fact that the female carries the em bryos on her back, either within a pouch of integument or in shallow depressions of the skin. The genera Flectonotus, Cast rotheca, and Amphignathodon are char acterized by pouches, while in Frit@iana, Crvptobatrachus, Ste fania and Henti phractus the embryos are carried in depressions of the skin. For a list of these frogs with locality and references of taxonomic interest see the work of Duellman (1976). Relatively little information is availal)le regarding reproduction and development in marsupial frogs. The relationship between mother and embryos has been studied in some detail in Gastrotheca riohanzbae, a species that carries the embryos in the potich up to the tadpole stage (see del Pino, Galarza, de Albtija, and Hum phries, 1975, for references). Among the species of Gastrotheca that carry the embryos to the young froglet stage, Gastrotheca ovif era is the best known (see Mertens, 1957, for a description of its life history and references). This report describes some features of oogenesis in 33 species of marsupial frogs that correspond to the described species of Ainphignathodon and Henzi phractus as listed by Duellman (1976), to two (of three) species of Flectonotus, one (of six) species of Stefania and 20 (of 32) species of Gastrotheca. In addi tion, the ovaries of three unnamed species of Gastrotlieca were also analyzed. The peculiarities of oogenesis have been studied in more detail in Flectonotns pvgmaeus, Gastrotheca ovif era and Gastrotheca sp., an unnanied species from Venezuela, since in these instances both living and preserved specimens were available. Living specimens of C. niarsupiata, G. excubitor, C. niertensi and C. plum bea were also

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34 citations

Journal Article•DOI•

Control of cell division and cell differentiation by deoxynucleotides in the early embryo of Xenopus laevis.

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Ulf Landström¹, Huguette Løvtrup-Rein¹, S Lovtrup¹•Institutions (1)

Umeå University¹

01 Dec 1975-Mechanisms of Development

TL;DR: It is proposed that the deoxyriboside triphosphates present in the egg of Xenopus laevis support the synchronous cell divisions occurring during the earliest phase of embryonic development and that, as long as synchrony prevails, the cells are prevented from undergoing differentiation.

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34 citations

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

...In Drosophila, it is difficult to see by light microscopy without specialized tags, and while obvious by electron microscopy, it is rather transient in comparison to its persistence in autonomously growing oocytes (Cox and Spradling 2003)....
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...Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019042 5 dy of Drosophila salivary gland cells have shown that the size attained depends on ploidy (Follette et al. 1998; Hayashi and Yamaguchi 1999)....
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...These features of the early cell cycle are seen in diverse settings—the rapidly dividing teleoblasts of annelid embryos, the syncytial mitotic cycles of Drosophila, the early divisions of sea urchin, and those of Xenopus....
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...There are numerous examples of huge cells: the Drosophila salivary gland cells, the cells of Ascaris (a nematode that has a volume a billion-fold bigger than C. elegans but the same cellular anatomy), the giant cells of Aplasia, and ciliates of extraordinary size....
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...Forexample, in Drosophila, a precursorcell called acystocyte divides four times to create an interconnected “cyst” of 16 cells that develops into an egg chamber in which 15 of the cells become highly polyploidy, and one cell, which will grow into the oocyte, arrests in meiotic prophase....
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Journal Article•DOI•

Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa

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Kevin J. Eckelbarger¹, R. Larson²•Institutions (2)

University of Maine¹, United States Fish and Wildlife Service²

01 Dec 1992-Marine Biology

TL;DR: The present study suggests that scyphozoans were among the first metazoans to develop ovarian accessory cells during their reproductive evolution and helps support the view that the Scyphozoa share a closer phylogenetic relationship with the Anthozoa than with the Hydrozoa.

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Abstract: Ovarian structure and oogenesis has been examined in six scyphozoan species including the semaeostome Diplumularis antarctica Maas, 1908 (collected in 1987 in McMurdo Sound, Antarctic), the rhizostomes Cassiopea xamachana Bigelow, 1892 (collected in Belize in 1988), and Stomolophus meleagris L. Agassiz, 1862 (collected in Ft. Pierce Inlet in 1988), and the coronates Periphylla periphylla (Peron and Lesueur, 1810), Nausithoe atlantica Broch, 1914 (both collected in the Bahamas in 1988), and Linuche unguiculata (Schwartz, 1788) (collected in Nassau Harbor, Bahama Islands in 1989). Based on these findings and information on five other scyphozoan species from additional literature sources, at least two fundamentally different types of ovaries exist in the Scyphozoa. In semaeosotome and rhizostome species, oocytes develop in close association with specialized gastrodermal cells called trophocytes which may serve a nutritive function. However, coronate species lack trophocytes and oocytes develop freely in the mesoglea. The ovaries of S. meleagris and L. unguiculata are used as models to represent the ultrastructural events occurring during oogenesis in species having trophocytes and those lacking them, respectively. In both L. unguiculata and S. meleagris, the ovaries arise as evaginations of the gastrodermis in the floor of interradial pouches. Germ cells appear to originate from endodermally-derived gastrodermal cells and migrate into the mesoglea prior to vitellogenesis. In L. unguiculata, the oocytes develop freely within the mesoglea throughout vitellogenesis, while in S. meleagris each oocyte maintains contact with specialized gastrodermal cells called trophocytes. In the vitellogenic oocytes of both species, numerous invaginations of the oolemma result in the formation of intraooplasmic channels throughout the ooplasm. These channels are intimately associated with cisternae of rough endoplasmic reticulum and may play some role in yolk precursor uptake by substantially increasing the surface area of the oocyte. Vitellogenesis is similar in both species and involves the autosynthetic activity of the Golge complex and rough endoplasmic reticulum, and the heterosynthetic incorporation of yolk precursors through receptor-mediated endocytosis. However, in the oocytes of S. meleagris, the trophocytes probably play a role in the transfer of nutrients from the gastrovascular cavity to the oocyte. The present study suggests that scyphozoans were among the first metazoans to develop ovarian accessory cells during their reproductive evolution. The trophocyte-oocyte association observed in some scyphozoans is similar to but structurally less complex than the trophonema-oocyte association described from anthozoans. Scyphozoan ovarian morphology helps support the view that the Scyphozoa share a closer phylogenetic relationship with the Anthozoa than with the Hydrozoa.

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32 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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...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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Journal Article•DOI•

Nanog co-regulated by Nodal/Smad2 and Oct4 is required for pluripotency in developing mouse epiblast.

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Liang Tso Sun¹, Shinpei Yamaguchi¹, Kunio Hirano¹, Tomoko Ichisaka¹, Takao Kuroda², Takashi Tada¹ - Show less +2 more•Institutions (2)

Kyoto University¹, Doshisha University²

15 Aug 2014-Developmental Biology

TL;DR: It is demonstrated that Nanog plays a key role in stabilizing Epiblast pluripotency mediated by Nodal/Smad2 signaling, which is involved in Nanog promoter switching in early developing embryos.

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32 citations

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

...These pluripotency factors are expressed in normal embryonic cells, and sustain pluripotency as the ICM cells of the blastocyst grow and proliferate before gastrulation (Marandel et al. 2012; Le Bin et al. 2014; Sun et al. 2014)....
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