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

  • 3,647
    views
  • 517
    downloads
  • 15
    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
    Michele Bertacchi, Gwendoline Maharaux ... Michèle Studer
    Research Article

    The morphogen FGF8 establishes graded positional cues imparting regional cellular responses via modulation of early target genes. The roles of FGF signaling and its effector genes remain poorly characterized in human experimental models mimicking early fetal telencephalic development. We used hiPSC-derived cerebral organoids as an in vitro platform to investigate the effect of FGF8 signaling on neural identity and differentiation. We found that FGF8 treatment increases cellular heterogeneity, leading to distinct telencephalic and mesencephalic-like domains that co-develop in multi-regional organoids. Within telencephalic domains, FGF8 affects the anteroposterior and dorsoventral identity of neural progenitors and the balance between GABAergic and glutamatergic neurons, thus impacting spontaneous neuronal network activity. Moreover, FGF8 efficiently modulates key regulators responsible for several human neurodevelopmental disorders. Overall, our results show that FGF8 signaling is directly involved in both regional patterning and cellular diversity in human cerebral organoids and in modulating genes associated with normal and pathological neural development.

    1. Cell Biology
    2. Developmental Biology
    Sarah Rubin, Ankit Agrawal ... Elazar Zelzer
    Research Article Updated

    Chondrocyte columns, which are a hallmark of growth plate architecture, play a central role in bone elongation. Columns are formed by clonal expansion following rotation of the division plane, resulting in a stack of cells oriented parallel to the growth direction. In this work, we analyzed hundreds of Confetti multicolor clones in growth plates of mouse embryos using a pipeline comprising 3D imaging and algorithms for morphometric analysis. Surprisingly, analysis of the elevation angles between neighboring pairs of cells revealed that most cells did not display the typical stacking pattern associated with column formation, implying incomplete rotation of the division plane. Morphological analysis revealed that although embryonic clones were elongated, they formed clusters oriented perpendicular to the growth direction. Analysis of growth plates of postnatal mice revealed both complex columns, composed of ordered and disordered cell stacks, and small, disorganized clusters located in the outer edges. Finally, correlation between the temporal dynamics of the ratios between clusters and columns and between bone elongation and expansion suggests that clusters may promote expansion, whereas columns support elongation. Overall, our findings support the idea that modulations of division plane rotation of proliferating chondrocytes determines the formation of either clusters or columns, a multifunctional design that regulates morphogenesis throughout pre- and postnatal bone growth. Broadly, this work provides a new understanding of the cellular mechanisms underlying growth plate activity and bone elongation during development.