Epiblast Stem Cell-based System Reveals Reprogramming Synergy of Germline Factors

Overview

Journal Cell Stem Cell

Publisher Cell Press

Specialty Cell Biology

Date 2012 Apr 10

PMID 22482507

Citations 76

Authors

Astrid Gillich

Siqin Bao

Nils Grabole

Katsuhiko Hayashi

Matthew W B Trotter

Vincent Pasque

Erna Magnusdottir

M Azim Surani

Affiliations

Soon will be listed here.

Abstract

Epigenetic reprogramming in early germ cells is critical toward the establishment of totipotency, but investigations of the germline events are intractable. An objective cell culture-based system could provide mechanistic insight on how the key determinants of primordial germ cells (PGCs), including Prdm14, induce reprogramming in germ cells to an epigenetic ground state. Here we show a Prdm14-Klf2 synergistic effect that can accelerate and enhance reversion of mouse epiblast stem cells (epiSCs) to a naive pluripotent state, including X reactivation and DNA demethylation. Notably, Prdm14 alone has little effect on epiSC reversion, but it enhances the competence for reprogramming and potentially PGC specification. Reprogramming of epiSCs by the combinatorial effect of Prdm14-Klf2 involves key epigenetic changes, which might have an analogous role in PGCs. Our study provides a paradigm toward a systematic analysis of how other key genes contribute to complex and dynamic events of reprogramming in the germline.

Citing Articles

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References

Hall J, Guo G, Wray J, Eyres I, Nichols J, Grotewold L . Oct4 and LIF/Stat3 additively induce Krüppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell. 2009; 5(6):597-609. DOI: 10.1016/j.stem.2009.11.003. View

Pasque V, Gillich A, Garrett N, Gurdon J . Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J. 2011; 30(12):2373-87. PMC: 3116279. DOI: 10.1038/emboj.2011.144. View

Ying Q, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J . The ground state of embryonic stem cell self-renewal. Nature. 2008; 453(7194):519-23. PMC: 5328678. DOI: 10.1038/nature06968. View

Hadjantonakis A, Cox L, Tam P, Nagy A . An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis. 2001; 29(3):133-40. DOI: 10.1002/gene.1016. View

Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K . Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature. 2009; 461(7268):1292-5. PMC: 3863718. DOI: 10.1038/nature08534. View

Chu L, Surani M, Jaenisch R, Zwaka T . Blimp1 expression predicts embryonic stem cell development in vitro. Curr Biol. 2011; 21(20):1759-65. PMC: 3203992. DOI: 10.1016/j.cub.2011.09.010. View

Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J . Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat Struct Mol Biol. 2010; 18(2):120-7. DOI: 10.1038/nsmb.2000. View

Yang J, van Oosten A, Theunissen T, Guo G, Silva J, Smith A . Stat3 activation is limiting for reprogramming to ground state pluripotency. Cell Stem Cell. 2010; 7(3):319-28. PMC: 3459098. DOI: 10.1016/j.stem.2010.06.022. View

Surani M, Hajkova P . Epigenetic reprogramming of mouse germ cells toward totipotency. Cold Spring Harb Symp Quant Biol. 2010; 75:211-8. DOI: 10.1101/sqb.2010.75.010. View

10.

Han D, Tapia N, Joo J, Greber B, Arauzo-Bravo M, Bernemann C . Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell. 2010; 143(4):617-27. DOI: 10.1016/j.cell.2010.10.015. View

11.

Brons I, Smithers L, Trotter M, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes S . Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature. 2007; 448(7150):191-5. DOI: 10.1038/nature05950. View

12.

Chia N, Chan Y, Feng B, Lu X, Orlov Y, Moreau D . A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature. 2010; 468(7321):316-20. DOI: 10.1038/nature09531. View

13.

Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M . Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet. 2008; 40(8):1016-22. DOI: 10.1038/ng.186. View

14.

Jiang J, Chan Y, Loh Y, Cai J, Tong G, Lim C . A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol. 2008; 10(3):353-60. DOI: 10.1038/ncb1698. View

15.

de Napoles M, Mermoud J, Wakao R, Tang Y, Endoh M, Appanah R . Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell. 2004; 7(5):663-76. DOI: 10.1016/j.devcel.2004.10.005. View

16.

Samavarchi-Tehrani P, Golipour A, David L, Sung H, Beyer T, Datti A . Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell. 2010; 7(1):64-77. DOI: 10.1016/j.stem.2010.04.015. View

17.

Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T . Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol. 2007; 26(1):101-6. DOI: 10.1038/nbt1374. View

18.

Hayashi K, Chuva de Sousa Lopes S, Tang F, Lao K, Surani M . Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell. 2008; 3(4):391-401. PMC: 3847852. DOI: 10.1016/j.stem.2008.07.027. View

19.

Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M . Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011; 146(4):519-32. DOI: 10.1016/j.cell.2011.06.052. View

20.

Vincent S, Dunn N, Sciammas R, Shapiro-Shalef M, Davis M, Calame K . The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development. 2005; 132(6):1315-25. DOI: 10.1242/dev.01711. View