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

Natalia Tapia; Peter Reinhardt; Annett Duemmler; Guangming Wu; Marcos J. Araúzo-Bravo; Daniel Esch; Boris Greber; Vlad Cojocaru; Cynthia Alexander Rascon; Akira Tazaki; Kevin Kump; Randal Voss; Elly M. Tanaka; Hans R. Schöler

doi:10.1038/ncomms2229

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

Natalia Tapia, Peter Reinhardt, Annett Duemmler, Guangming Wu, Marcos J. Araúzo-Bravo, Daniel Esch, Boris Greber, Vlad Cojocaru, Cynthia Alexander Rascon, Akira Tazaki, Kevin Kump, Randal Voss, Elly M. Tanaka, Hans R. Schöler

Neuroscience

Research output: Contribution to journal › Article › peer-review

59 Scopus citations

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.

Original language	English
Article number	1279
Journal	Nature Communications
Volume	3
DOIs	https://doi.org/10.1038/ncomms2229
State	Published - 2012

Bibliographical note

Funding Information:
We are indebted to all members of the Schöler and Tanaka laboratories for fruitful discussion of the results. We also thank Rhea Brintrup, Martina Bleidi≈el, Bärbel Schäfer, Boris Burr, Sandra Heising, Heino Andreas, Sabine Moegel and Beate Gruhl for technical assistance; T. Kitamura for providing the pMX retroviral vector; Andreas Hermann and Alexander Storch from the Dresden University of Technology for providing the human fibroblasts; and Alex Kalinka and Felipe Merino for advice in the phylogenetic analysis. We thank Areti Malapetsas for editing the manuscript. This work was supported by the Max Planck Society, the Center for Regenerative Therapies, and the DFG grants SCHO 340/7-1, TA274/2-2, TA274/4-1 and SPP1356.

Funding

We are indebted to all members of the Schöler and Tanaka laboratories for fruitful discussion of the results. We also thank Rhea Brintrup, Martina Bleidi≈el, Bärbel Schäfer, Boris Burr, Sandra Heising, Heino Andreas, Sabine Moegel and Beate Gruhl for technical assistance; T. Kitamura for providing the pMX retroviral vector; Andreas Hermann and Alexander Storch from the Dresden University of Technology for providing the human fibroblasts; and Alex Kalinka and Felipe Merino for advice in the phylogenetic analysis. We thank Areti Malapetsas for editing the manuscript. This work was supported by the Max Planck Society, the Center for Regenerative Therapies, and the DFG grants SCHO 340/7-1, TA274/2-2, TA274/4-1 and SPP1356.

Funders	Funder number
Center for Regenerative Therapies
NIH Office of the Director	R24OD010435
Deutsche Forschungsgemeinschaft	SCHO 340/7-1, SPP1356, TA274/4-1, TA274/2-2
Fritz-Haber-Institut der Max-Planck-Gesellschaft

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/ncomms2229

Cite this

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title = "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.",

author = "Natalia Tapia and Peter Reinhardt and Annett Duemmler and Guangming Wu and Ara{\'u}zo-Bravo, {Marcos J.} and Daniel Esch and Boris Greber and Vlad Cojocaru and Rascon, {Cynthia Alexander} and Akira Tazaki and Kevin Kump and Randal Voss and Tanaka, {Elly M.} and Sch{\"o}ler, {Hans R.}",

note = "Funding Information: We are indebted to all members of the Sch{\"o}ler and Tanaka laboratories for fruitful discussion of the results. We also thank Rhea Brintrup, Martina Bleidi≈el, B{\"a}rbel Sch{\"a}fer, Boris Burr, Sandra Heising, Heino Andreas, Sabine Moegel and Beate Gruhl for technical assistance; T. Kitamura for providing the pMX retroviral vector; Andreas Hermann and Alexander Storch from the Dresden University of Technology for providing the human fibroblasts; and Alex Kalinka and Felipe Merino for advice in the phylogenetic analysis. We thank Areti Malapetsas for editing the manuscript. This work was supported by the Max Planck Society, the Center for Regenerative Therapies, and the DFG grants SCHO 340/7-1, TA274/2-2, TA274/4-1 and SPP1356.",

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doi = "10.1038/ncomms2229",

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AU - Tapia, Natalia

AU - Reinhardt, Peter

AU - Duemmler, Annett

AU - Wu, Guangming

AU - Araúzo-Bravo, Marcos J.

AU - Esch, Daniel

AU - Greber, Boris

AU - Cojocaru, Vlad

AU - Rascon, Cynthia Alexander

AU - Tazaki, Akira

AU - Kump, Kevin

AU - Voss, Randal

AU - Tanaka, Elly M.

AU - Schöler, Hans R.

N1 - Funding Information: We are indebted to all members of the Schöler and Tanaka laboratories for fruitful discussion of the results. We also thank Rhea Brintrup, Martina Bleidi≈el, Bärbel Schäfer, Boris Burr, Sandra Heising, Heino Andreas, Sabine Moegel and Beate Gruhl for technical assistance; T. Kitamura for providing the pMX retroviral vector; Andreas Hermann and Alexander Storch from the Dresden University of Technology for providing the human fibroblasts; and Alex Kalinka and Felipe Merino for advice in the phylogenetic analysis. We thank Areti Malapetsas for editing the manuscript. This work was supported by the Max Planck Society, the Center for Regenerative Therapies, and the DFG grants SCHO 340/7-1, TA274/2-2, TA274/4-1 and SPP1356.

PY - 2012

Y1 - 2012

N2 - 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.

AB - 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.

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

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

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