Transcription Coactivator Cited1 Acts As an Inducer of Trophoblast-like State from Mouse Embryonic Stem Cells Through the Activation of BMP Signaling

Overview

Journal Cell Death Dis

Specialties Cell Biology
General Medicine

Date 2018 Sep 13

PMID 30206204

Citations 8

Authors

Yanli Xu

Xinlong Luo

Zhuoqing Fang

Xiaofeng Zheng

Yanwu Zeng

Chaonan Zhu

Junjie Gu

Fan Tang

Yanqin Hu

Guang Hu

Ying Jin

Hui Li

Affiliations

Soon will be listed here.

Abstract

Trophoblast lineages, precursors of the placenta, are essential for post-implantation embryo survival. However, the regulatory network of trophoblast development remains incompletely understood. Here, we report that Cited1, a transcription coactivator, is a robust inducer for trophoblast-like state from mouse embryonic stem cells (ESCs). Depletion of Cited1 in ESCs compromises the trophoblast lineage specification induced by BMP signaling. In contrast, overexpression of Cited1 in ESCs induces a trophoblast-like state with elevated expression of trophoblast marker genes in vitro and generation of trophoblastic tumors in vivo. Furthermore, global transcriptome profile analysis indicates that ectopic Cited1 activates a trophoblast-like transcriptional program in ESCs. Mechanistically, Cited1 interacts with Bmpr2 and Smad4 to activate the Cited1-Bmpr2-Smad1/5/8 axis in the cytoplasm and Cited1-Smad4-p300 complexes in the nucleus, respectively. Collectively, our results show that Cited1 plays an important role in regulating trophoblast lineage specification through activating the BMP signaling pathway.

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References

Marchand M, Horcajadas J, Esteban F, McElroy S, Fisher S, Giudice L . Transcriptomic signature of trophoblast differentiation in a human embryonic stem cell model. Biol Reprod. 2011; 84(6):1258-71. DOI: 10.1095/biolreprod.110.086413. View

Galvin K, Travis E, Yee D, Magnuson T, Vivian J . Nodal signaling regulates the bone morphogenic protein pluripotency pathway in mouse embryonic stem cells. J Biol Chem. 2010; 285(26):19747-56. PMC: 2888385. DOI: 10.1074/jbc.M109.077347. View

Schulz L, Ezashi T, Das P, Westfall S, Livingston K, Roberts R . Human embryonic stem cells as models for trophoblast differentiation. Placenta. 2007; 29 Suppl A:S10-6. PMC: 2330081. DOI: 10.1016/j.placenta.2007.10.009. View

Plisov S, Tsang M, Shi G, Boyle S, Yoshino K, Dunwoodie S . Cited1 is a bifunctional transcriptional cofactor that regulates early nephronic patterning. J Am Soc Nephrol. 2005; 16(6):1632-44. DOI: 10.1681/ASN.2004060476. View

Tolkunova E, Cavaleri F, Eckardt S, Reinbold R, Christenson L, Scholer H . The caudal-related protein cdx2 promotes trophoblast differentiation of mouse embryonic stem cells. Stem Cells. 2005; 24(1):139-44. DOI: 10.1634/stemcells.2005-0240. View

Das P, Ezashi T, Schulz L, Westfall S, Livingston K, Roberts R . Effects of fgf2 and oxygen in the bmp4-driven differentiation of trophoblast from human embryonic stem cells. Stem Cell Res. 2009; 1(1):61-74. PMC: 2634289. DOI: 10.1016/j.scr.2007.09.004. View

Ran F, Hsu P, Wright J, Agarwala V, Scott D, Zhang F . Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013; 8(11):2281-2308. PMC: 3969860. DOI: 10.1038/nprot.2013.143. View

Vong Q, Liu Z, Yoo J, Chen R, Xie W, Sharov A . A role for borg5 during trophectoderm differentiation. Stem Cells. 2010; 28(6):1030-8. PMC: 2957878. DOI: 10.1002/stem.428. View

Ten Dijke P, Hill C . New insights into TGF-beta-Smad signalling. Trends Biochem Sci. 2004; 29(5):265-73. DOI: 10.1016/j.tibs.2004.03.008. View

10.

Rodriguez T, Sparrow D, Scott A, Withington S, Preis J, Michalicek J . Cited1 is required in trophoblasts for placental development and for embryo growth and survival. Mol Cell Biol. 2003; 24(1):228-44. PMC: 303371. DOI: 10.1128/MCB.24.1.228-244.2004. View

11.

Evans M, Kaufman M . Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981; 292(5819):154-6. DOI: 10.1038/292154a0. View

12.

Koh K, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J . Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell. 2011; 8(2):200-13. PMC: 3134318. DOI: 10.1016/j.stem.2011.01.008. View

13.

Ahmed N, Shioda T, Coser K, Ichihashi M, Ueda M . Aberrant expression of MSG1 transcriptional activator in human malignant melanoma in vivo. Pigment Cell Res. 2001; 14(2):140-3. View

14.

Yahata T, Shao W, Endoh H, Hur J, Coser K, Sun H . Selective coactivation of estrogen-dependent transcription by CITED1 CBP/p300-binding protein. Genes Dev. 2001; 15(19):2598-612. PMC: 312794. DOI: 10.1101/gad.906301. View

15.

Liu J, Luo X, Xu Y, Gu J, Tang F, Jin Y . Single-stranded DNA binding protein Ssbp3 induces differentiation of mouse embryonic stem cells into trophoblast-like cells. Stem Cell Res Ther. 2016; 7(1):79. PMC: 4884356. DOI: 10.1186/s13287-016-0340-1. View

16.

Xu H, Liao B, Zhang Q, Wang B, Li H, Zhong X . Wwp2, an E3 ubiquitin ligase that targets transcription factor Oct-4 for ubiquitination. J Biol Chem. 2004; 279(22):23495-503. DOI: 10.1074/jbc.M400516200. View

17.

Shioda T, Fenner M, Isselbacher K . MSG1 and its related protein MRG1 share a transcription activating domain. Gene. 1998; 204(1-2):235-41. DOI: 10.1016/s0378-1119(97)00551-9. View

18.

Rhee C, Lee B, Beck S, Anjum A, Cook K, Popowski M . Arid3a is essential to execution of the first cell fate decision via direct embryonic and extraembryonic transcriptional regulation. Genes Dev. 2014; 28(20):2219-32. PMC: 4201284. DOI: 10.1101/gad.247163.114. View

19.

Meniel V, Song F, Phesse T, Young M, Poetz O, Parry L . Cited1 deficiency suppresses intestinal tumorigenesis. PLoS Genet. 2013; 9(8):e1003638. PMC: 3731217. DOI: 10.1371/journal.pgen.1003638. View

20.

Ralston A, Cox B, Nishioka N, Sasaki H, Chea E, Rugg-Gunn P . Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development. 2010; 137(3):395-403. DOI: 10.1242/dev.038828. View