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•

Nuclear metabolism of ribosomal RNA in growing, methionine-limited, and ethionine-treated HeLa cells.

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Stanley F. Wolf, David Schlessinger

14 Jun 1977-Biochemistry

77 citations

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

...Furthermore, there are a lot of ribosomes in even an ordinary cell, roughly several million (Blobel and Potter 1967; Wolf and Schlessinger 1977), a few orders of magnitude more than most abundant mRNAs....
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Journal Article•DOI•

Geminin Escapes Degradation in G1 of Mouse Pluripotent Cells and Mediates the Expression of Oct4, Sox2, and Nanog

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Valerie S. Yang, Stephanie A. Carter, Sarah J. Hyland, Kikuë Tachibana-Konwalski¹, Ronald A. Laskey, Michael A Gonzalez - Show less +2 more•Institutions (1)

University of Oxford¹

26 Apr 2011-Current Biology

TL;DR: It is shown that geminin is present in G1 phase of mouse pluripotent cells in contrast to somatic cells, where anaphase-promoting complex/cyclosome (APC/C)-mediated proteasomal destruction removes geminIn.

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75 citations

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

...Furthermore, oscillations of numerous key cell-cycle regulators are greatly dampened, such that there is peculiarly high cyclin:Cdk activity in interphase (Savatier et al. 1996; Fujii-Yamamoto et al. 2005; Yang et al. 2011; van der Laan et al. 2013)....
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Journal Article•DOI•

Development of polyembryonic insects: a major departure from typical insect embryogenesis

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Miodrag Grbic¹, Lisa M. Nagy², Micheal R. Strand¹•Institutions (2)

University of Wisconsin-Madison¹, University of Arizona²

01 Apr 1998-Development Genes and Evolution

TL;DR: The early development of polyembryonic wasps, which likely evolved in association with a shift in life history to endoparasitism, shows several analogies with mammalian embryogenesis, including early separation of extra Embryonic and embryonic cell lineages, formation of a morula and embryonic compaction.

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Abstract: The parasitic wasp Copidosoma floridanum represents the most extreme form of polyembryonic development known, forming up to 2000 embryos from a single egg. To understand the mechanisms of embryonic patterning in polyembryonic wasps and the evolutionary changes that led to this form of development we have analyzed embryonic development at the cellular level using confocal and scanning electron microscopy. C. floridanum embryogenesis can be divided into three phases: (1) early cleavage that leads to formation of a primary morula, (2) a proliferative phase that involves partitioning of embryonic cells into thousands of morulae, and (3) morphogenesis whereby individual embryos develop into larvae. This developmental program represents a major departure from typical insect embryogenesis, and we describe several features of morphogenesis unusual for insects. The early development of polyembryonic wasps, which likely evolved in association with a shift in life history to endoparasitism, shows several analogies with mammalian embryogenesis, including early separation of extraembryonic and embryonic cell lineages, formation of a morula and embryonic compaction. However, the late morphogenesis of polyembryonic wasps proceeds in a fashion conserved in all insects. Collectively, this suggests a lack of developmental constraints in early development, but a strong conservation of the phylotypic stage.

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72 citations

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

...This lifestyle has evolved independently numerous times (Grbić et al. 1998; Grbić 2000; Wiegmann et al. 2011), and a diversity of changes in early development are found among the species with this lifestyle (Grbić et al....
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...The endoparasitic wasps lay their eggs inside the larvae of bigger insects where they develop in the nutrient-rich hemolymph (Grbić et al. 1998; Grbić 2000; Wiegmann et al. 2011)....
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...2011), and a diversity of changes in early development are found among the species with this lifestyle (Grbić et al. 1998; Grbić 2000; Wiegmann et al. 2011)....
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...This is the result of a remarkable adaptation in which the embryo twins repeatedly in a process called polyembryony (Grbić et al. 1998; Grbić 2000; Wiegmann et al. 2011)....
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Journal Article•DOI•

Mechanism and regulation of Cdc25/Twine protein destruction in embryonic cell-cycle remodeling.

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Jeffrey A. Farrell¹, Patrick H. O'Farrell¹•Institutions (1)

University of California, San Francisco¹

21 Jan 2013-Current Biology

TL;DR: It is proposed that the developmentally regulated destruction of Twine protein is a critical switch that contributes to the cell-cycle change at the MBT, including the addition of a G2 phase and onset of late replication.

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71 citations

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

...For example, inhibitory phosphorylation leads to a decline in activity of the cell-cycle kinase, Cdk1, prolongs S phase, and introduces a G2 phase at the MBT in Drosophila (Edgar and O’Farrell 1990; Farrell and O’Farrell 2013)....
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Journal Article•DOI•

Balbiani body, nuage and sponge bodies – The germ plasm pathway players

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Malgorzata Kloc¹, Izabela Jędrzejowska², Waclaw Tworzydlo³, Szczepan M. Bilinski³•Institutions (3)

Houston Methodist Hospital¹, University of Wrocław², Jagiellonian University³

01 Jul 2014-Arthropod Structure & Development

TL;DR: The present article reviews the current knowledge on morphology, molecular composition and functioning of these organelles in main lineages of arthropods and different ovary types on the backdrop of data derived from the studies of the model vertebrate species.

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68 citations

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

...This structure, which is found in the oocytes of a wide range of animals, is seen as a differentiated area of cytoplasm that can be detected early in oogenesis, just as precursor cells are committing to oogenesis (Kloc et al. 2014)....
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...Mitochondrial morphology and DNA labeling argue that Balbiani body mitochondria proliferate (Chase and Dawid 1972; Webb and Smith 1977; Kloc et al. 2014)....
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...This stage often persists for months as the oocyte enlarges, and studies in Xenopus showed that oocyte transcripts accumulate during this period (Gall 2012; Kloc et al. 2014)....
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...…to several functions—storing mRNAs for the future embryo, specifying the vegetal or posterior pole of the egg, defining the germline, and protecting against infectious DNA elements by housing an immunity system based on a category of small RNAs, piRNAs (Marlow and Mullins 2008; Kloc et al. 2014)....
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...and identification of molecular constituents have tied nuage not to one, but to several functions—storing mRNAs for the future embryo, specifying the vegetal or posterior pole of the egg, defining the germline, and protecting against infectious DNA elements by housing an immunity system based on a category of small RNAs, piRNAs (Marlow and Mullins 2008; Kloc et al. 2014)....
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