Induced 2C Expression and Implantation-Competent Blastocyst-like Cysts from Primed Pluripotent Stem Cells

Overview

Journal Stem Cell Reports

Publisher Cell Press

Specialty Cell Biology

Date 2019 Aug 13

PMID 31402336

Citations 37

Authors

Cody Kime

Hiroshi Kiyonari

Satoshi Ohtsuka

Eiko Kohbayashi

Michio Asahi

Shinya Yamanaka

Masayo Takahashi

Kiichiro Tomoda

Affiliations

Soon will be listed here.

Abstract

Soon after fertilization, the few totipotent cells of mammalian embryos diverge to form a structure called the blastocyst (BC). Although numerous cell types, including germ cells and extended-pluripotency stem cells, have been developed from pluripotent stem cells (PSCs) in vitro, generating functional BCs only from PSCs remains elusive. Here, we describe induced self-organizing 3D BC-like cysts (iBLCs) generated from mouse PSC culture. Resembling natural BCs, iBLCs have a blastocoel-like cavity and were formed with outer cells expressing trophectoderm lineage markers and with inner cells expressing pluripotency markers. iBLCs transplanted to pseudopregnant mice uteruses implanted, induced decidualization, and exhibited growth and development before resorption, demonstrating that iBLCs are implantation competent. iBLC precursor intermediates required the transcription factor Prdm14 and concomitantly activated the totipotency-related cleavage-stage MERVL reporter and 2C genes. Thus, our system may contribute to the understanding of molecular mechanisms underpinning totipotency, embryogenesis, and implantation.

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References

Hirate Y, Hirahara S, Inoue K, Kiyonari H, Niwa H, Sasaki H . Par-aPKC-dependent and -independent mechanisms cooperatively control cell polarity, Hippo signaling, and cell positioning in 16-cell stage mouse embryos. Dev Growth Differ. 2015; 57(8):544-56. PMC: 11520972. DOI: 10.1111/dgd.12235. View

Rivron N, Frias-Aldeguer J, Vrij E, Boisset J, Korving J, Vivie J . Blastocyst-like structures generated solely from stem cells. Nature. 2018; 557(7703):106-111. DOI: 10.1038/s41586-018-0051-0. View

Tesar P, Chenoweth J, Brook F, Davies T, Evans E, Mack D . New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature. 2007; 448(7150):196-9. DOI: 10.1038/nature05972. View

Macfarlan T, Gifford W, Agarwal S, Driscoll S, Lettieri K, Wang J . Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev. 2011; 25(6):594-607. PMC: 3059833. DOI: 10.1101/gad.2008511. 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

Qin H, Hejna M, Liu Y, Percharde M, Wossidlo M, Blouin L . YAP Induces Human Naive Pluripotency. Cell Rep. 2016; 14(10):2301-12. PMC: 4807727. DOI: 10.1016/j.celrep.2016.02.036. View

Yang S, Yuan Q, Niu M, Hou J, Zhu Z, Sun M . BMP4 promotes mouse iPS cell differentiation to male germ cells via Smad1/5, Gata4, Id1 and Id2. Reproduction. 2016; 153(2):211-220. DOI: 10.1530/REP-16-0292. View

Ralston A, Rossant J . Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol. 2007; 313(2):614-29. DOI: 10.1016/j.ydbio.2007.10.054. View

Burton A, Muller J, Tu S, Padilla-Longoria P, Guccione E, Torres-Padilla M . Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Rep. 2013; 5(3):687-701. DOI: 10.1016/j.celrep.2013.09.044. View

10.

Kime C, Sakaki-Yumoto M, Goodrich L, Hayashi Y, Sami S, Derynck R . Autotaxin-mediated lipid signaling intersects with LIF and BMP signaling to promote the naive pluripotency transcription factor program. Proc Natl Acad Sci U S A. 2016; 113(44):12478-12483. PMC: 5098653. DOI: 10.1073/pnas.1608564113. View

11.

Hubner K, Fuhrmann G, Christenson L, Kehler J, Reinbold R, De La Fuente R . Derivation of oocytes from mouse embryonic stem cells. Science. 2003; 300(5623):1251-6. DOI: 10.1126/science.1083452. View

12.

Kime C, Kiyonari H, Ohtsuka S, Kohbayashi E, Asahi M, Yamanaka S . Induced 2C Expression and Implantation-Competent Blastocyst-like Cysts from Primed Pluripotent Stem Cells. Stem Cell Reports. 2019; 13(3):485-498. PMC: 6739768. DOI: 10.1016/j.stemcr.2019.07.011. View

13.

Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y . The landscape of accessible chromatin in mammalian preimplantation embryos. Nature. 2016; 534(7609):652-7. DOI: 10.1038/nature18606. View

14.

Ohinata Y, Tsukiyama T . Establishment of trophoblast stem cells under defined culture conditions in mice. PLoS One. 2014; 9(9):e107308. PMC: 4159327. DOI: 10.1371/journal.pone.0107308. View

15.

Czechanski A, Byers C, Greenstein I, Schrode N, Donahue L, Hadjantonakis A . Derivation and characterization of mouse embryonic stem cells from permissive and nonpermissive strains. Nat Protoc. 2014; 9(3):559-74. PMC: 4112089. DOI: 10.1038/nprot.2014.030. View

16.

Parchem R, Ye J, Judson R, LaRussa M, Krishnakumar R, Blelloch A . Two miRNA clusters reveal alternative paths in late-stage reprogramming. Cell Stem Cell. 2014; 14(5):617-31. PMC: 4305531. DOI: 10.1016/j.stem.2014.01.021. View

17.

Mochida K, Hasegawa A, Otaka N, Hama D, Furuya T, Yamaguchi M . Devising assisted reproductive technologies for wild-derived strains of mice: 37 strains from five subspecies of Mus musculus. PLoS One. 2014; 9(12):e114305. PMC: 4254977. DOI: 10.1371/journal.pone.0114305. View

18.

Cha J, Sun X, Dey S . Mechanisms of implantation: strategies for successful pregnancy. Nat Med. 2012; 18(12):1754-67. PMC: 6322836. DOI: 10.1038/nm.3012. View

19.

Chen W, Jia W, Wang K, Zhou Q, Leng Y, Duan T . Retinoic acid regulates germ cell differentiation in mouse embryonic stem cells through a Smad-dependent pathway. Biochem Biophys Res Commun. 2012; 418(3):571-7. DOI: 10.1016/j.bbrc.2012.01.078. View

20.

Saiz N, Plusa B . Early cell fate decisions in the mouse embryo. Reproduction. 2012; 145(3):R65-80. DOI: 10.1530/REP-12-0381. View