Characterisation of the finch embryo supports evolutionary conservation of the naïve stage of development in amniotes

Abstract

Innate pluripotency of mouse embryos transits from naïve to primed state as the inner cell mass (ICM) differentiates into epiblast. In vitro, their counterparts are embryonic (ESCs) and epiblast stem cells (EpiSCs) respectively. Activation of the FGF signalling cascade results in mouse ESCs differentiating into mEpiSCs, indicative of its requirement in the shift between these states. However, only mouse ESCs correspond to the naïve state; ESCs from other mammals and from chick show primed state characteristics. Thus, the significance of the naïve state is unclear. Here, we use zebra finch as a model for comparative ESC studies. The finch blastoderm has mESC-like properties, while chick blastoderm exhibits EpiSC features. In the absence of FGF signalling, finch cells retained expression of pluripotent markers, which were lost in cells from chick or aged finch epiblasts. Our data suggest that the naïve state of pluripotency is evolutionarily conserved among amniotes.

Article and author information

Author details

  1. Siu-Shan Mak

    Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Cantas Alev

    Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Hiroki Nagai

    Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Anna Wrabel

    Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Yoko Matsuoka

    Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Akira Honda

    Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Guojun Sheng

    Laboratory for Early Embryogenesis, RIKEN Center for Developmental Biology, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Raj K Ladher

    Laboratory for Sensory Development, RIKEN Center for Developmental Biology, Kobe, Japan
    For correspondence
    rajladher@ncbs.res.in
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Mak et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,674
    views
  • 522
    downloads
  • 1
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Siu-Shan Mak
  2. Cantas Alev
  3. Hiroki Nagai
  4. Anna Wrabel
  5. Yoko Matsuoka
  6. Akira Honda
  7. Guojun Sheng
  8. Raj K Ladher
(2015)
Characterisation of the finch embryo supports evolutionary conservation of the naïve stage of development in amniotes
eLife 4:e07178.
https://doi.org/10.7554/eLife.07178

Share this article

https://doi.org/10.7554/eLife.07178

Further reading

    1. Developmental Biology
    Cora Demler, John C Lawlor ... Natasza A Kurpios
    Research Article

    Correct intestinal morphogenesis depends on the early embryonic process of gut rotation, an evolutionarily conserved program in which a straight gut tube elongates and forms into its first loops. However, the gut tube requires guidance to loop in a reproducible manner. The dorsal mesentery (DM) connects the gut tube to the body and directs the lengthening gut into stereotypical loops via left-right (LR) asymmetric cellular and extracellular behavior. The LR asymmetry of the DM also governs blood and lymphatic vessel formation for the digestive tract, which is essential for prenatal organ development and postnatal vital functions including nutrient absorption. Although the genetic LR asymmetry of the DM has been extensively studied, a divider between the left and right DM has yet to be identified. Setting up LR asymmetry for the entire body requires a Lefty1+ midline barrier to separate the two sides of the embryo, without it, embryos have lethal or congenital LR patterning defects. Individual organs including the brain, heart, and gut also have LR asymmetry, and while the consequences of left and right signals mixing are severe or even lethal, organ-specific mechanisms for separating these signals remain poorly understood. Here, we uncover a midline structure composed of a transient double basement membrane, which separates the left and right halves of the embryonic chick DM during the establishment of intestinal and vascular asymmetries. Unlike other basement membranes of the DM, the midline is resistant to disruption by intercalation of Netrin4 (Ntn4). We propose that this atypical midline forms the boundary between left and right sides and functions as a barrier necessary to establish and protect organ asymmetry.

    1. Developmental Biology
    Valeria Sulzyk, Ludmila Curci ... Patricia S Cuasnicu
    Research Article

    Numerous reports showed that the epididymis plays key roles in the acquisition of sperm fertilizing ability but its contribution to embryo development remains less understood. Female mice mated with males with simultaneous mutations in Crisp1 and Crisp3 genes exhibited normal in vivo fertilization but impaired embryo development. In this work, we found that this phenotype was not due to delayed fertilization, and it was observed in eggs fertilized by epididymal sperm either in vivo or in vitro. Of note, eggs fertilized in vitro by mutant sperm displayed impaired meiotic resumption unrelated to Ca2+ oscillations defects during egg activation, supporting potential sperm DNA defects. Interestingly, cauda but not caput epididymal mutant sperm exhibited increased DNA fragmentation, revealing that DNA integrity defects appear during epididymal transit. Moreover, exposing control sperm to mutant epididymal fluid or to Ca2+-supplemented control fluid significantly increased DNA fragmentation. This, together with the higher intracellular Ca2+ levels detected in mutant sperm, supports a dysregulation in Ca2+ homeostasis within the epididymis and sperm as the main factor responsible for embryo development failure. These findings highlight the contribution of the epididymis beyond fertilization and identify CRISP1 and CRISP3 as novel factors essential for sperm DNA integrity and early embryo development.