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•

"Alien" wasps and evolution of development.

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Miodrag Grbic¹•Institutions (1)

University of Western Ontario¹

01 Oct 2000-BioEssays

TL;DR: A comparative analysis of early developmental programs in a group of parasitic wasps reveals that closely related species can undergo dramatic evolutionary shifts in their patterns of embryogenesis.

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Abstract: A comparative analysis of early developmental programs in a group of parasitic wasps reveals that closely related species can undergo dramatic evolutionary shifts in their patterns of embryogenesis. Developmental changes detected include alterations in early cleavage divisions, the establishment of embryonic anteroposterior polarity and modifications of the segmentation gene hierarchy described from Drosophila. These changes appear to be adaptations to parasitic development, taking place within the body of the host. Wasps illustrate a surprising plasticity in their early development and embryogenesis. The alterations associated with different parasitic strategies suggest that ecological adaptations may have profound influences on developmental processes in animals. BioEssays 22:920–932, 2000. © 2000 John Wiley & Sons, Inc.

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31 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•

Connecting cell behavior to patterning: lessons from the cell cycle.

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Peter Follette¹, Patrick H. O'Farrell¹•Institutions (1)

University of California, San Francisco¹

07 Feb 1997-Cell

TL;DR: The lessons learned from studies of the cell cycle are generalizable and provide a paradigm for an understanding of many aspects of cell behavior required for morphogenesis; the authors will discuss here the regulation of several such behaviors.

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31 citations

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

...In part, this is a progressive transition with additional zygotic functions coming into play as persisting maternal functions are successively eliminated (Wieschaus 1996; Follette and O’Farrell 1997)....
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Journal Article•DOI•

Growth and its control in early mammalian development.

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M H L Snow¹•Institutions (1)

Medical Research Council¹

01 Sep 1981-British Medical Bulletin

28 citations

Journal Article•DOI•

nanog 5′-upstream sequence, DNA methylation, and expression in gametes and early embryo reveal striking differences between teleosts and mammals

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Lucie Marandel¹, Catherine Labbé¹, Julien Bobe¹, Pierre-Yves Le Bail¹•Institutions (1)

Institut national de la recherche agronomique¹

15 Jan 2012-Gene

TL;DR: Striking differences in expression and DNA methylation patterns in gametes and during early development and in upstream region features between teleosts and mammals are revealed that are consistent with the hypothesis of a rapid evolution of the Nanog gene in vertebrates, at least in some lineages.

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25 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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...As discussed below, even though these mechanisms are set in a different context in mammalian development, an understanding of the ancestral mechanism will give us deeper insight into this process in mammals (Cañon et al. 2011; Sánchez-Sánchez et al. 2011; Marandel et al. 2012; Lee et al. 2013)....
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Journal Article•DOI•

Ultrastructure of the Ovary and Oogenesis in the Methane-Seep Mollusc Bathynerita naticoidea (Gastropoda: Neritidae) from the Louisiana Slope

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Kevin J. Eckelbarger, Craig M. Young

23 Jan 1997-Invertebrate Biology

25 citations