Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency
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The support of pluripotent cells over time is an essential feature of development. In eutherian embryos, pluripotency is maintained from naïve states in peri-implantation to primed pluripotency at gastrulation. To understand how these states emerged, we reconstruct the evolutionary trajectory of the Pou5 gene family, which contains the central pluripotency factor OCT4. By coupling evolutionary sequence analysis with functional studies in mouse embryonic stem cells, we find that the ability of POU5 proteins to support pluripotency originated in the gnathostome lineage, prior to the generation of two paralogues, Pou5f1 and Pou5f3 via gene duplication. In osteichthyans, retaining both genes, the paralogues differ in their support of naïve and primed pluripotency. The specialization of these duplicates enables the diversification of function in self-renewal and differentiation. By integrating sequence evolution, cell phenotypes, developmental contexts and structural modelling, we pinpoint OCT4 regions sufficient for naïve pluripotency and describe their adaptation over evolutionary time.
| Originalsprog | Engelsk |
|---|---|
| Artikelnummer | 5537 |
| Tidsskrift | Nature Communications |
| Vol/bind | 13 |
| Udgave nummer | 1 |
| Antal sider | 21 |
| ISSN | 2041-1723 |
| DOI | |
| Status | Udgivet - 2022 |
Bibliografisk note
Funding Information:
We thank Gillian Morrison for POU5 plasmids, Moisés Mallo for python Pou5f1 mRNA sequence, Keisuke Kaji, Kumiko A. Iwabuchi and Maria Kraft for technical help in iPSCs generation, Yasunori Murakami and Chris Amemiya for assisting with preliminary cyclostome POU5 analysis, Charlotte Bouleau and Charline Jamin for technical help in ScPou5f1 ISH, the late Andrew Johnson for inspirational discussion, William Hamilton for bioinformatics advice and the entire Brickman laboratory members for critical discussion and reading of this manuscript. We also thank the Oceanological Observatory Aquariology Service of Banyuls sur Mer for care of catsharks and EMBRC-France for the support of marine infrastructure. We thank Jutta Bulkescher, Anup Shrestha and the reNEW Imaging Platform for training, technical expertise, support and the use of microscopes; Gelo dela Cruz, Paul van Dieken and the reNEW Flow Cytometry Platform for technical expertise, support and the use of instruments; Javier Martin Gonzalez for assistance with mouse work; Eduardo Fernandez Rebollo, Michelle Paulsen, Angeliki Meligkova and reNEW Tissue Culture Lab Facilities, for support of tissue culture. This work was supported by University of Copenhagen studentship (to W.S.), Lundbeck Foundation Grant (to J.M.B, R198-2015-412, to M.L. R264-2017-2915, and to M.W. R264-2017-3212), région Bretagne doctoral fellowship (to B.G.G.) and AsymBrain ANR grant (to S.M., ANR-16-CE13-0013-02). Work in the Novo Nordisk Foundation (NNF) Center for Stem Cell Medicine (reNEW) is funded by the NNF, grant number NNF21CC0073729 and previously NNF17CC0027852. Work in the NNF Center for Protein Research (CPR) is funded by the NNF, grant number NNF14CC0001. G.M, is a member of the Integrative Structural Biology Cluster (ISBUC) at the University of Copenhagen.
Funding Information:
We thank Gillian Morrison for POU5 plasmids, Moisés Mallo for python Pou5f1 mRNA sequence, Keisuke Kaji, Kumiko A. Iwabuchi and Maria Kraft for technical help in iPSCs generation, Yasunori Murakami and Chris Amemiya for assisting with preliminary cyclostome POU5 analysis, Charlotte Bouleau and Charline Jamin for technical help in ScPou5f1 ISH, the late Andrew Johnson for inspirational discussion, William Hamilton for bioinformatics advice and the entire Brickman laboratory members for critical discussion and reading of this manuscript. We also thank the Oceanological Observatory Aquariology Service of Banyuls sur Mer for care of catsharks and EMBRC-France for the support of marine infrastructure. We thank Jutta Bulkescher, Anup Shrestha and the reNEW Imaging Platform for training, technical expertise, support and the use of microscopes; Gelo dela Cruz, Paul van Dieken and the reNEW Flow Cytometry Platform for technical expertise, support and the use of instruments; Javier Martin Gonzalez for assistance with mouse work; Eduardo Fernandez Rebollo, Michelle Paulsen, Angeliki Meligkova and reNEW Tissue Culture Lab Facilities, for support of tissue culture. This work was supported by University of Copenhagen studentship (to W.S.), Lundbeck Foundation Grant (to J.M.B, R198-2015-412, to M.L. R264-2017-2915, and to M.W. R264-2017-3212), région Bretagne doctoral fellowship (to B.G.G.) and AsymBrain ANR grant (to S.M., ANR-16-CE13-0013-02). Work in the Novo Nordisk Foundation (NNF) Center for Stem Cell Medicine (reNEW) is funded by the NNF, grant number NNF21CC0073729 and previously NNF17CC0027852. Work in the NNF Center for Protein Research (CPR) is funded by the NNF, grant number NNF14CC0001. G.M, is a member of the Integrative Structural Biology Cluster (ISBUC) at the University of Copenhagen.
Publisher Copyright:
© 2022, The Author(s).
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