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Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins.

ABSTRACT: The evolutionary origins of the gene network underlying cellular pluripotency, a central theme in developmental biology, have yet to be elucidated. In mammals, Oct4 is a factor crucial in the reprogramming of differentiated cells into induced pluripotent stem cells. The Oct4 and Pou2 genes evolved from a POU class V gene ancestor, but it is unknown whether pluripotency induced by Oct4 gene activity is a feature specific to mammals or was already present in ancestral vertebrates. Here we report that different vertebrate Pou2 and Oct4 homologues can induce pluripotency in mouse and human fibroblasts and that the inability of zebrafish Pou2 to establish pluripotency is not representative of all Pou2 genes, as medaka Pou2 and axolotl Pou2 are able to reprogram somatic cells into pluripotent cells. Therefore, our results indicate that induction of pluripotency is not a feature specific to mammals, but existed in the Oct4/Pou2 common ancestral vertebrate.

SUBMITTER: Tapia N

PROVIDER: S-EPMC4892893 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins.

Tapia Natalia N Reinhardt Peter P Duemmler Annett A Wu Guangming G Araúzo-Bravo Marcos J MJ Esch Daniel D Greber Boris B Cojocaru Vlad V Rascon Cynthia Alexander CA Tazaki Akira A Kump Kevin K Voss Randal R Tanaka Elly M EM Schöler Hans R HR

Nature communications 20120101

The evolutionary origins of the gene network underlying cellular pluripotency, a central theme in developmental biology, have yet to be elucidated. In mammals, Oct4 is a factor crucial in the reprogramming of differentiated cells into induced pluripotent stem cells. The Oct4 and Pou2 genes evolved from a POU class V gene ancestor, but it is unknown whether pluripotency induced by Oct4 gene activity is a feature specific to mammals or was already present in ancestral vertebrates. Here we report t ...[more]

PMID: 23232409

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Project description:Pluripotency is the capacity of early embryonic cells to make all the future lineages of the organism, and the existence of a pluripotent population of cells is important to both germ cell function and the pool of progenitor cells that enable vertebrate development to proceed over time through the process of gastrulation. Oct4, a class V POU transcription factor, is required for maintenance of pluripotency in embryonic stem cells (ESCs) and induction of pluripotency via transcription factor reprogramming. Homologues of Oct4 have been identified in other gnathostomes and classified into two different paralogues: POU5F1 and POU5F3. Here we provide evidence that these proteins are probably derived from a single POUV gene through ancient whole genome duplication events. To approach this issue, we compared the functional conservation and divergence of different POUV proteins in their capacity to support naïve pluripotency in mouse ESCs. We found a strong correlation between POU5F1 activity in naïve pluripotency and the regulation of germ cell specification programs. In contrast, POU5F3 exhibited reduced capacity to support naïve ESCs and its activity in ESCs correlated with the expression of genes associated with pre-gastrulation stages, or primed pluripotency. We detected evidence of this functional segregation as early as Sarcopterygian ancestors, based on the activities of coelacanth POUV proteins. Furthermore, we were able to identify earlier POUV homologues in lamprey and shark, indicating that the earliest point at which mammalian-level pluripotency of both POUV paralogues emerged is between the osteichthyan-chondrichthyan split and the gnathostome-cyclostome split.Taken together, our work highlights the evolutionary history of POUV activities across jawed vertebrates, suggesting that evolutionary pressure has facilitated maintenance of both paralogues over long periods of evolutionary history. In species with both paralogues, subfunctionalization of these proteins appears conserved. However, in many branches of vertebrate evolution, one of these paralogues is lost, suggesting a high level of plasticity in function and precarious balance between retaining both proteins and the overall levels of POUV activity in different developmental systems. While the conserved subfunctionalization of POUV activities evolved at some point just before the appearance of tetrapods, the additional divergent activities of this protein family appear to have evolved independently in each vertebrate lineage after gnathostome radiation.

Dataset Information

Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins.

Publications

Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins.

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