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Embryonic stem cell potency fluctuates with endogenous retrovirus activity

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  • Todd S. Macfarlan

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA
    Present address: Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, USA.)

  • Wesley D. Gifford

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Shawn Driscoll

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Karen Lettieri

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Helen M. Rowe

    (School of Life Sciences, Ecole Polytechnique Federale de Lausanne (EPFL), 1015 Lausanne, Switzerland)

  • Dario Bonanomi

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Amy Firth

    (Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Oded Singer

    (Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

  • Didier Trono

    (School of Life Sciences, Ecole Polytechnique Federale de Lausanne (EPFL), 1015 Lausanne, Switzerland)

  • Samuel L. Pfaff

    (Howard Hughes Medical Institute, Gene Expression Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines, La Jolla, California 92037, USA)

Abstract

Embryonic stem (ES) cells are derived from blastocyst-stage embryos and are thought to be functionally equivalent to the inner cell mass, which lacks the ability to produce all extraembryonic tissues. Here we identify a rare transient cell population within mouse ES and induced pluripotent stem (iPS) cell cultures that expresses high levels of transcripts found in two-cell (2C) embryos in which the blastomeres are totipotent. We genetically tagged these 2C-like ES cells and show that they lack the inner cell mass pluripotency proteins Oct4 (also known as Pou5f1), Sox2 and Nanog, and have acquired the ability to contribute to both embryonic and extraembryonic tissues. We show that nearly all ES cells cycle in and out of this privileged state, which is partially controlled by histone-modifying enzymes. Transcriptome sequencing and bioinformatic analyses showed that many 2C transcripts are initiated from long terminal repeats derived from endogenous retroviruses, suggesting this foreign sequence has helped to drive cell-fate regulation in placental mammals.

Suggested Citation

  • Todd S. Macfarlan & Wesley D. Gifford & Shawn Driscoll & Karen Lettieri & Helen M. Rowe & Dario Bonanomi & Amy Firth & Oded Singer & Didier Trono & Samuel L. Pfaff, 2012. "Embryonic stem cell potency fluctuates with endogenous retrovirus activity," Nature, Nature, vol. 487(7405), pages 57-63, July.
    • Handle: RePEc:nat:nature:v:487:y:2012:i:7405:d:10.1038_nature11244
    DOI: 10.1038/nature11244
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    Cited by:

    1. Rabajante, Jomar Fajardo & Talaue, Cherryl Ortega, 2015. "Equilibrium switching and mathematical properties of nonlinear interaction networks with concurrent antagonism and self-stimulation," Chaos, Solitons & Fractals, Elsevier, vol. 73(C), pages 166-182.
    2. Belén de la Hera & Jezabel Varadé & Marta García-Montojo & José Ramón Lamas & Ana de la Encarnación & Rafael Arroyo & Benjamín Fernández-Gutiérrez & Roberto Álvarez-Lafuente & Elena Urcelay, 2013. "Role of the Human Endogenous Retrovirus HERV-K18 in Autoimmune Disease Susceptibility: Study in the Spanish Population and Meta-Analysis," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-7, April.
    3. Zhengyi Li & Haiyan Xu & Jiaqun Li & Xiao Xu & Junjiao Wang & Danya Wu & Jiateng Zhang & Juan Liu & Ziwei Xue & Guankai Zhan & Bobby Cheng Peow Tan & Di Chen & Yun-Shen Chan & Huck Hui Ng & Wanlu Liu , 2023. "Selective binding of retrotransposons by ZFP352 facilitates the timely dissolution of totipotency network," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Hua Yu & Zhen Sun & Tianyu Tan & Hongru Pan & Jing Zhao & Ling Zhang & Jiayu Chen & Anhua Lei & Yuqing Zhu & Lang Chen & Yuyan Xu & Yaxin Liu & Ming Chen & Jinghao Sheng & Zhengping Xu & Pengxu Qian &, 2021. "rRNA biogenesis regulates mouse 2C-like state by 3D structure reorganization of peri-nucleolar heterochromatin," Nature Communications, Nature, vol. 12(1), pages 1-21, December.

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