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Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency

Author

Listed:
  • Woranop Sukparangsi

    (University of Copenhagen
    Burapha University)

  • Elena Morganti

    (University of Copenhagen)

  • Molly Lowndes

    (University of Copenhagen)

  • Hélène Mayeur

    (CNRS, Sorbonne Université, Biologie Intégrative des Organismes Marins, UMR7232)

  • Melanie Weisser

    (University of Copenhagen)

  • Fella Hammachi

    (University of Edinburgh)

  • Hanna Peradziryi

    (University of Copenhagen)

  • Fabian Roske

    (University of Copenhagen)

  • Jurriaan Hölzenspies

    (University of Copenhagen)

  • Alessandra Livigni

    (University of Edinburgh)

  • Benoit Gilbert Godard

    (CNRS, Sorbonne Université, UPMC Univ Paris 06, FR2424, Development and Evolution of Vertebrates Group, Station Biologique
    CNRS, Sorbonne Université, Laboratoire de Biologie du Développement de Villefranche, UMR7009)

  • Fumiaki Sugahara

    (Division of Biology, Hyogo College of Medicine)

  • Shigeru Kuratani

    (Laboratory for Evolutionary Morphology, RIKEN Center for Biosystems Dynamics Research (BDR))

  • Guillermo Montoya

    (University of Copenhagen)

  • Stephen R. Frankenberg

    (University of Melbourne)

  • Sylvie Mazan

    (CNRS, Sorbonne Université, Biologie Intégrative des Organismes Marins, UMR7232)

  • Joshua M. Brickman

    (University of Copenhagen)

Abstract

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.

Suggested Citation

  • Woranop Sukparangsi & Elena Morganti & Molly Lowndes & Hélène Mayeur & Melanie Weisser & Fella Hammachi & Hanna Peradziryi & Fabian Roske & Jurriaan Hölzenspies & Alessandra Livigni & Benoit Gilbert G, 2022. "Evolutionary origin of vertebrate OCT4/POU5 functions in supporting pluripotency," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32481-z
    DOI: 10.1038/s41467-022-32481-z
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