Long Noncoding RNA Sponges Mmu-miR-139-5p to Modulate Functions in Mouse ESCs and Embryos

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2020 Sep 29

PMID 32991228

Citations 4

Authors

Dongfang Xie

Man Tong

Baolong Xia

Guihai Feng

Leyun Wang

Ang Li

Guanzheng Luo

Haifeng Wan

Zeyu Zhang

Hao Zhang

Yun-Gui Yang

Qi Zhou

Meng Wang

Xiu-Jie Wang

Affiliations

Soon will be listed here.

Abstract

The pluripotency of embryonic stem cells (ESCs) is controlled by a multilayer regulatory network, of which the key factors include core pluripotency genes and , and multiple microRNAs (miRNAs). Recently, long noncoding RNAs (lncRNAs) have been discovered as a class of new regulators for ESCs, and some lncRNAs could function as competing endogenous RNAs (ceRNAs) to regulate mRNAs by competitively binding to miRNAs. Here, we identify mmu-miR-139-5p as a new regulator for by targeting 3' untranslated region (UTR) to repress expression in mouse ESCs and embryos. Such regulation could be released by an ESC-specifically expressed ceRNA named . The expression of is activated by OCT4, SOX2, as well as NANOG through promoter binding. Downregulation of reduces abundance, which leads to decreased pluripotency of mouse ESCs and embryonic lethality. These results reveal as a new regulator for in mouse ESCs, and uncover a feed-forward regulatory loop of through the participation of .

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References

Chakraborty D, Kappei D, Theis M, Nitzsche A, Ding L, Paszkowski-Rogacz M . Combined RNAi and localization for functionally dissecting long noncoding RNAs. Nat Methods. 2012; 9(4):360-2. DOI: 10.1038/nmeth.1894. View

Hu L, Xu Z, Hu B, Lu Z . COME: a robust coding potential calculation tool for lncRNA identification and characterization based on multiple features. Nucleic Acids Res. 2016; 45(1):e2. PMC: 5224497. DOI: 10.1093/nar/gkw798. View

Luo G, Hafner M, Shi Z, Brown M, Feng G, Tuschl T . Genome-wide annotation and analysis of zebra finch microRNA repertoire reveal sex-biased expression. BMC Genomics. 2012; 13:727. PMC: 3585881. DOI: 10.1186/1471-2164-13-727. View

Thomson J, Itskovitz-Eldor J, Shapiro S, Waknitz M, Swiergiel J, Marshall V . Embryonic stem cell lines derived from human blastocysts. Science. 1998; 282(5391):1145-7. DOI: 10.1126/science.282.5391.1145. View

Boyer L, Lee T, Cole M, Johnstone S, Levine S, Zucker J . Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005; 122(6):947-56. PMC: 3006442. DOI: 10.1016/j.cell.2005.08.020. View

Xu N, Papagiannakopoulos T, Pan G, Thomson J, Kosik K . MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell. 2009; 137(4):647-58. DOI: 10.1016/j.cell.2009.02.038. View

Hu W, Zhang W, Li F, Guo F, Chen A . miR-139 is up-regulated in osteoarthritis and inhibits chondrocyte proliferation and migration possibly via suppressing EIF4G2 and IGF1R. Biochem Biophys Res Commun. 2016; 474(2):296-302. DOI: 10.1016/j.bbrc.2016.03.164. View

Arrial R, Togawa R, Brigido M . Screening non-coding RNAs in transcriptomes from neglected species using PORTRAIT: case study of the pathogenic fungus Paracoccidioides brasiliensis. BMC Bioinformatics. 2009; 10:239. PMC: 2731755. DOI: 10.1186/1471-2105-10-239. View

Rashid F, Shah A, Shan G . Long Non-coding RNAs in the Cytoplasm. Genomics Proteomics Bioinformatics. 2016; 14(2):73-80. PMC: 4880952. DOI: 10.1016/j.gpb.2016.03.005. View

10.

Zou F, Mao R, Yang L, Lin S, Lei K, Zheng Y . Targeted deletion of miR-139-5p activates MAPK, NF-κB and STAT3 signaling and promotes intestinal inflammation and colorectal cancer. FEBS J. 2016; 283(8):1438-52. DOI: 10.1111/febs.13678. View

11.

Guo H, Hu X, Ge S, Qian G, Zhang J . Regulation of RAP1B by miR-139 suppresses human colorectal carcinoma cell proliferation. Int J Biochem Cell Biol. 2012; 44(9):1465-72. DOI: 10.1016/j.biocel.2012.05.015. View

12.

Young R . Control of the embryonic stem cell state. Cell. 2011; 144(6):940-54. PMC: 3099475. DOI: 10.1016/j.cell.2011.01.032. View

13.

Miyanari Y, Torres-Padilla M . Control of ground-state pluripotency by allelic regulation of Nanog. Nature. 2012; 483(7390):470-3. DOI: 10.1038/nature10807. View

14.

Jaenisch R, Young R . Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell. 2008; 132(4):567-82. PMC: 4142810. DOI: 10.1016/j.cell.2008.01.015. View

15.

Langmead B, Trapnell C, Pop M, Salzberg S . Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25. PMC: 2690996. DOI: 10.1186/gb-2009-10-3-r25. View

16.

Yan Y, Yang X, Li T, Gu K, Hao J, Zhang Q . Significant differences of function and expression of microRNAs between ground state and serum-cultured pluripotent stem cells. J Genet Genomics. 2017; 44(4):179-189. DOI: 10.1016/j.jgg.2017.01.005. View

17.

Mintz P, Saetrom P, Reebye V, Lundbaek M, Lao K, Rossi J . MicroRNA-181a* Targets Nanog in a Subpopulation of CD34(+) Cells Isolated From Peripheral Blood. Mol Ther Nucleic Acids. 2013; 1:e34. PMC: 3437805. DOI: 10.1038/mtna.2012.29. View

18.

Liu L, Luo G, Yang W, Zhao X, Zheng Q, Lv Z . Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem. 2010; 285(25):19483-90. PMC: 2885227. DOI: 10.1074/jbc.M110.131995. View

19.

Trapnell C, Williams B, Pertea G, Mortazavi A, Kwan G, van Baren M . Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28(5):511-5. PMC: 3146043. DOI: 10.1038/nbt.1621. View

20.

Tay Y, Zhang J, Thomson A, Lim B, Rigoutsos I . MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature. 2008; 455(7216):1124-8. DOI: 10.1038/nature07299. View