HBL1 Is a Human Long Noncoding RNA That Modulates Cardiomyocyte Development from Pluripotent Stem Cells by Counteracting MIR1

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2017 Aug 23

PMID 28829943

Citations 33

Authors

Juli Liu

Yang Li

Bo Lin

Yi Sheng

Lei Yang

Affiliations

Soon will be listed here.

Abstract

Cardiogenesis processes in human and animals have differential dynamics, suggesting the existence of species-specific regulators during heart development. However, it remains a challenge to discover the human-specific cardiac regulatory genes, given that most coding genes are conserved. Here, we report the identification of a human-specific long noncoding RNA, Heart Brake LncRNA 1 (HBL1), which regulates cardiomyocyte development from human induced pluripotent stem cells (hiPSCs). Overexpression of HBL1 repressed, whereas knockdown and knockout of HBL1 increased, cardiomyocyte differentiation from hiPSCs. HBL1 physically interacted with MIR1 in an AGO2 complex. Disruption of MIR1 binding sites in HBL1 showed an effect similar to that of HBL1 knockout. SOX2 bound to HBL1 promoter and activated its transcription. Knockdown of SOX2 in hiPSCs led to decreased HBL1 expression and increased cardiomyocyte differentiation efficiency. Thus, HBL1 plays a modulatory role in fine-tuning human-specific cardiomyocyte development by forming a regulatory network with SOX2 and MIR1.

Citing Articles

GATA3-Driven ceRNA Network in Lung Adenocarcinoma Bone Metastasis Progression and Therapeutic Implications.

Liu Y, Shen S, Wang X, Chen H, Ren W, Wei H Cancers (Basel). 2025; 17(3).

PMID: 39941924 PMC: 11816722. DOI: 10.3390/cancers17030559.

Mef2c- and Nkx2-5-Divergent Transcriptional Regulation of Chick WT1_76127 and Mouse Gm14014 lncRNAs and Their Implication in Epicardial Cell Migration.

Cano-Carrillo S, Garcia-Padilla C, Aranega A, Lozano-Velasco E, Franco D Int J Mol Sci. 2024; 25(23).

PMID: 39684625 PMC: 11640978. DOI: 10.3390/ijms252312904.

Monkeypox virus protein H3L induces injuries in human and mouse.

Chen S, Huang G, Liu J Cell Death Dis. 2024; 15(8):607.

PMID: 39168969 PMC: 11339448. DOI: 10.1038/s41419-024-06990-2.

Dynamic changes in LINC00458/HBL1 lncRNA expression during hiPSC differentiation to cardiomyocytes.

Maciak P, Suder A, Wadas J, Aronimo F, Maiuri P, Bochenek M Sci Rep. 2024; 14(1):109.

PMID: 38167488 PMC: 10761834. DOI: 10.1038/s41598-023-49753-3.

The roles of long noncoding RNAs in atrial fibrillation.

Beylerli O, Ju J, Beilerli A, Gareev I, Shumadalova A, Ilyasova T Noncoding RNA Res. 2023; 8(4):542-549.

PMID: 37602317 PMC: 10432912. DOI: 10.1016/j.ncrna.2023.08.004.

References

Peltier H, Latham G . Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA. 2008; 14(5):844-52. PMC: 2327352. DOI: 10.1261/rna.939908. View

Kattman S, Witty A, Gagliardi M, Dubois N, Niapour M, Hotta A . Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell. 2011; 8(2):228-40. DOI: 10.1016/j.stem.2010.12.008. View

Tay Y, Rinn J, Pandolfi P . The multilayered complexity of ceRNA crosstalk and competition. Nature. 2014; 505(7483):344-52. PMC: 4113481. DOI: 10.1038/nature12986. View

Urban A, Neukirchen S, Jaeger K . A rapid and efficient method for site-directed mutagenesis using one-step overlap extension PCR. Nucleic Acids Res. 1997; 25(11):2227-8. PMC: 146699. DOI: 10.1093/nar/25.11.2227. View

Ludwig T, Bergendahl V, Levenstein M, Yu J, Probasco M, Thomson J . Feeder-independent culture of human embryonic stem cells. Nat Methods. 2006; 3(8):637-46. DOI: 10.1038/nmeth902. View

Quinn J, Chang H . Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2015; 17(1):47-62. DOI: 10.1038/nrg.2015.10. View

Batista P, Chang H . Long noncoding RNAs: cellular address codes in development and disease. Cell. 2013; 152(6):1298-307. PMC: 3651923. DOI: 10.1016/j.cell.2013.02.012. View

Wang L, Park H, Dasari S, Wang S, Kocher J, Li W . CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013; 41(6):e74. PMC: 3616698. DOI: 10.1093/nar/gkt006. View

Lu T, Lin B, Li Y, Arora A, Han L, Cui C . Overexpression of microRNA-1 promotes cardiomyocyte commitment from human cardiovascular progenitors via suppressing WNT and FGF signaling pathways. J Mol Cell Cardiol. 2013; 63:146-54. PMC: 4268488. DOI: 10.1016/j.yjmcc.2013.07.019. View

10.

Li Y, Lin B, Yang L . Comparative transcriptomic analysis of multiple cardiovascular fates from embryonic stem cells predicts novel regulators in human cardiogenesis. Sci Rep. 2015; 5:9758. PMC: 4440522. DOI: 10.1038/srep09758. View

11.

Ma M, Chu B, Zhang Y, Weng M, Qin Y, Gong W . Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218-5p. Cell Death Dis. 2015; 6:e1583. PMC: 4669740. DOI: 10.1038/cddis.2014.541. View

12.

Lu M, Tang B, Zeng S, Hu C, Xie R, Wu Y . Long noncoding RNA BC032469, a novel competing endogenous RNA, upregulates hTERT expression by sponging miR-1207-5p and promotes proliferation in gastric cancer. Oncogene. 2015; 35(27):3524-34. DOI: 10.1038/onc.2015.413. View

13.

Ivey K, Muth A, Arnold J, King F, Yeh R, Fish J . MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell. 2008; 2(3):219-29. PMC: 2293325. DOI: 10.1016/j.stem.2008.01.016. View

14.

Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T . Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell. 2004; 15(2):185-97. DOI: 10.1016/j.molcel.2004.07.007. View

15.

Takeuchi J, Bruneau B . Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature. 2009; 459(7247):708-11. PMC: 2728356. DOI: 10.1038/nature08039. View

16.

Xia T, Liao Q, Jiang X, Shao Y, Xiao B, Xi Y . Long noncoding RNA associated-competing endogenous RNAs in gastric cancer. Sci Rep. 2014; 4:6088. PMC: 4133709. DOI: 10.1038/srep06088. View

17.

Toko H, Zhu W, Takimoto E, Shiojima I, Hiroi Y, Zou Y . Csx/Nkx2-5 is required for homeostasis and survival of cardiac myocytes in the adult heart. J Biol Chem. 2002; 277(27):24735-43. DOI: 10.1074/jbc.M107669200. View

18.

Turchinovich A, Burwinkel B . Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol. 2012; 9(8):1066-75. PMC: 3551861. DOI: 10.4161/rna.21083. View

19.

Cong L, Zhang F . Genome engineering using CRISPR-Cas9 system. Methods Mol Biol. 2014; 1239:197-217. DOI: 10.1007/978-1-4939-1862-1_10. View

20.

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