Characterization of the finch embryo supports evolutionary conservation of the naive stage of development in amniotes

Abstract

Innate pluripotency of mouse embryos transits from naive to primed state as the inner cell mass differentiates into epiblast. In vitro, their counterparts are embryonic (ESCs) and epiblast stem cells (EpiSCs), respectively. Activation of the FGF signaling 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 naive state; ESCs from other mammals and from chick show primed state characteristics. Thus, the significance of the naive state is unclear. In this study, 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 signaling, finch cells retained expression of pluripotent markers, which were lost in cells from chick or aged finch epiblasts. Our data suggest that the naive state of pluripotency is evolutionarily conserved among amniotes.

DOI: http://dx.doi.org/10.7554/eLife.07178.001

eLife digest

In animals, stem cells divide to give rise to other cells that have specialized roles in the body. ‘Pluripotent’ stem cells—which are able to produce cells of any type—can be obtained from young mouse embryos. Once grown in the laboratory, these cells are called naive embryonic stem cells (ESCs) and their discovery has been vitally important for understanding how mammals develop. ESCs also have considerable medical potential because they could be used to repair or replace tissues that have been lost to injury or disease.

A family of proteins called fibroblast growth factors (FGFs) triggers naive ESCs to mature into another class of stem cell that are ‘primed’ to only produce particular types of cells. Curiously, the stem cells that have been collected from other mammal embryos are already in this primed state. Therefore, biologists wonder whether the naive state is exclusive to mice embryos, or whether it is present in other animals but has so far remained undetected.

The development of chick and other bird embryos shares many parallels with that of mammals. However, embryos in chicken eggs do not contain naive ESCs. It is possible that this is due to chicken eggs being laid when the embryos have reached a later stage in development where the naive stem cells have already matured into the primed cells. Here, Mak et al. compared the stem cells in chick embryos to those from another bird called the zebra finch.

The experiments show that the finch embryos contain stem cells that share several features with mouse ESCs. In particular, these finch cells continue to express genes that are required for the naive state to be maintained in the absence of FGF. On the other hand, these genes are switched off in cells from chick embryos and in older zebra finch stem cells.

Mak et al.'s findings show that finch eggs are laid at an earlier stage of embryo development than chicken eggs. The experiments also suggest that both birds and mammals have naive pluripotent stem cells during the early stages of embryo development. In future, the zebra finch could be used as a model to study stem cells and other aspects of animal development.

DOI: http://dx.doi.org/10.7554/eLife.07178.002