LncRNAs are Involved in the Process of Atherosclerosis at Diverse Levels

Liang, Shiyi; Xv, Weicheng; Li, Chijian; Huang, Yuxiang; Qian, Ge; Yan, Yuxiang; Zou, Hequn; Li, Yongqiang

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Arquivos Brasileiros de Cardiologia

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Review Article • Arq. Bras. Cardiol. 118 (6) • 2022 • https://doi.org/10.36660/abc.20201383 copy

LncRNAs are Involved in the Process of Atherosclerosis at Diverse Levels

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Atherosclerosis is the most common cause of cardiovascular disease globally, associated with a high incidence of clinical events. Accumulating evidence has elucidated that long non-coding RNAs (lncRNAs) as a novel class of transcripts with critical roles in the pathophysiological processes of atherosclerosis. In this review, we summarize the recent progress of lncRNAs in the development of atherosclerosis. We mainly describe the diverse regulatory mechanisms of lncRNAs at the transcriptional and post-transcriptional levels. This study may provide helpful insights about lncRNAs as therapeutic targets or biomarkers for atherosclerosis treatment.

Keywords
LnRNAs; Emzymes; Enzyme Inhibitors; Endothelial Cells; Lipoproteins, VLDL; RNA Interference

	lncRNAs	Mechanism	Effect		References
Cells function			Proliferation	Apoptosis
Endothelial cells (ECs)	MALAT1	MALAT1-Pc2 (CBX4)-E2F1	⁺ (+) represents prompt or increase, and		³⁸38 Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD, et al. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell. 2011;147(4):773-88. doi: 10.1016/j.cell.2011.08.054. https://doi.org/10.1016/j.cell.2011.08.0...
	GAS5	GAS5 - ceRNA (miR-21)	⁻ (−) represents prevent or decrease.	⁺ (+) represents prompt or increase, and	⁷⁵75 Shen Z, She Q. Association Between the Deletion Allele of Ins/Del Polymorphism (Rs145204276) in the Promoter Region of GAS5 with the risk of atherosclerosis. Cell Physiol Biochem. 2018;49(4):1431-43. doi: 10.1159/000493447 https://doi.org/10.1159/000493447...
	HOTTIP	TNF-α/PDGFBB-HOTTIP-β-catenin	⁺ (+) represents prompt or increase, and		⁴⁷47 Liao B, Chen R, Lin F, Mai A, Chen J, Li H, et al. Long non-coding RNA HOTTIP promotes endothelial cell proliferation and migration via activation of the Wnt/β-catenin pathway.J Cell Biochem. 2018;19(3):2797-805. doi: 10.1002/jcb.26448. https://doi.org/10.1002/jcb.26448...
	MALAT1	ceRNA (miR-22-3p)		⁻ (−) represents prevent or decrease.	⁶⁰60 Tang Y, Jin X, Xiang Y, Chen Y, Shen CX, Zhang YC, et al. The lncRNA MALAT1 protects the endothelium against ox-LDL-induced dysfunction via upregulating the expression of the miR-22-3p target genes CXCR2 and AKT. FEBS Lett. 2015;589(20Pt8):3189-96. doi: 10.1016/j.febslet.2015.08.046. https://doi.org/10.1016/j.febslet.2015.0...
	TUG1	ceRNA (miR-26a)		⁺ (+) represents prompt or increase, and	⁷¹71 Chen C, Cheng G, Yang X, Li C, Shi R, Zhao N. Tanshinol suppresses endothelial cells apoptosis in mice with atherosclerosis via lncRNA TUG1 up-regulating the expression of miR-26a. Am J TRanslat Res.2016;8(7):2981-91. PMID: 27508018
Macrophages, Smooth muscular cells	ANRIL	Bind with CBX7 and SUZ12	⁺ (+) represents prompt or increase, and	⁻ (−) represents prevent or decrease.	³²32 Visel A, Zhu Y, May D, Afzal V, Gong E, Attanasio C, et al. Targeted deletion of the 9p21 non-coding coronary artery disease risk interval in mice. Nature. 2010;464(7287):409-12. doi: 10.1038/nature08801 https://doi.org/10.1038/nature08801...
	NEAT1	NEAT1-WDR5-SM-specific genes	⁺ (+) represents prompt or increase, and		⁴⁴44 ASI Ahmed ASI, Dong K, Liu J, Wen T, Yu L, Xu F, et al. NEAT1Long non-coding RNA (nuclear paraspeckle assembly transcript 1) is critical for phenotypic switching of vascular smooth muscle cells. Proc the Nat Acad Scienc (USA) 2018; 37: E8660-67. doi: 10.3892/mmr.2017.8211 https://doi.org/10.3892/mmr.2017.8211...
	LincRNA-p21	lincRNA-p21-MDM2/ p300-p53	⁺ (+) represents prompt or increase, and	⁻ (−) represents prevent or decrease.	⁴⁵45 Wu G, Cai J, Han Y, Chen J, Huang ZP, Chen C, et al. LincRNA-p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity. Circulation. 2014; 130(17):1452-65. doi: 10.1161/CIRCULATIONAHA.114.011675 https://doi.org/10.1161/CIRCULATIONAHA.1...
	HAS2	remodeling chromatin structure	⁺ (+) represents prompt or increase, and		⁴⁹49 van den Boom M, Sarbia M, von Wnuck Lipinski K, Mann P, Meyer-Kirchrath J, Rauch BH, et al. Differential regulation of hyaluronic acid synthase isoforms in human saphenous vein smooth muscle cells: possible implications for vein graft stenosis. Circ Res.2006;98(1):36-44. doi: 10.1161/01.RES.0000199263.67107.c0. https://doi.org/10.1161/01.RES.000019926... ,⁵⁰50 Viola M, Karousou E, D’Angelo ML, Moretto P, Caon I, Luca G, et al. Extracellular Matrix in Atherosclerosis: Hyaluronan and Proteoglycans Insights. Curr Med Chem. 2016;23(26):2958-71. doi: 10.2174/0929867323666160607104602. https://doi.org/10.2174/0929867323666160...
	RP11-714G18.1	upregulate LRP2BP expression		⁻ (−) represents prevent or decrease.	⁵³53 Zhang Y, Zheng L, Xu BM, Tang WH, Ye ZD, Huang C, et al. LncRNA-RP11-714G18.1 suppresses vascular cell migration via directly targeting LRP2BP. Imm cell Biol. 2018; 2:175-89. doi: 10.1016/j.eururo.2018.07.032. https://doi.org/10.1016/j.eururo.2018.07...
	H19	ceRNA (miR-148b)	⁺ (+) represents prompt or increase, and	⁻ (−) represents prevent or decrease.	⁶⁶66 Zhang L, Cheng H, Yue Y, Li S, Zhang D,He R. H19 knockdown suppresses proliferation and induces apoptosis by regulating miR-148b/WNT/β-catenin in ox-LDL -stimulated vascular smooth muscle cells. J Biomed Sci.2018;25(1):11.. 2018; 1: 11. doi: 10.1186/s12929-018-0418-4. https://doi.org/10.1186/s12929-018-0418-...
	MIAT	ceRNA (miR-181b)	⁺ (+) represents prompt or increase, and	⁻ (−) represents prevent or decrease.	⁶⁹69 Zhong X, Ma X, Zhang L, Li Y, He R. MIAT promotes proliferation and hinders apoptosis by modulating miR-181b/STAT3 axis in ox-LDL-induced atherosclerosis cell models. Biomed Pharmacother Biomed.2018;97: 1078-85. doi: 10.1016/j.biopha.2017.11.052. https://doi.org/10.1016/j.biopha.2017.11...

	lncRNAs	Mechanism	Effect	References
Lipid accumulation	MALAT1	MALAT1-CD36-lipid uptake	⁺ (+) represents prompt or increase, and	⁴⁵45 Wu G, Cai J, Han Y, Chen J, Huang ZP, Chen C, et al. LincRNA-p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity. Circulation. 2014; 130(17):1452-65. doi: 10.1161/CIRCULATIONAHA.114.011675 https://doi.org/10.1161/CIRCULATIONAHA.1...
	NEAT1	NEAT1-CD36-lipid uptake	⁻ (−) represents prevent or decrease.	⁴¹41 Huangfu N, Xu Z, Zheng W, Wang Y, Cheng J, Chen X. LncRNA MALAT1 regulates oxLDL-induced CD36 expression via activating β-catenin. Bioch Biopohys Res Comm. 2018;3:2111-7. (ISSN: 1090-2104)
	MeXis	LXR-MeXis-Abca1	⁻ (−) represents prevent or decrease.	⁴⁶46 Sallam T, Jones M, Thomas BJ, Wu X, Gilliland T, Qian K, et al. Transcriptional regulation of macrophage cholesterol efflux and atherogenesis by a long non-coding RNA. Nat Med. 2018;24(3):304-12. doi: 10.1038/nm.4479. https://doi.org/10.1038/nm.4479...
	H19	ceRNA (miR-130b)	⁻ (−) represents prevent or decrease.	⁶⁵65 Han Y, Ma J, Wang J, Wang L Silencing of H19 inhibits the adipogenesis and inflammation response in ox-LDL-treated Raw264.7 cells by up-regulating miR-130b. Mol Immunol.2018;93:107-14. doi: 10.1016/j.molimm.2017.11.017 https://doi.org/10.1016/j.molimm.2017.11...
	TUG1	ceRNA (miR-133a)	⁺ (+) represents prompt or increase, and	⁷²72 Zhang L, Cheng H, Yue Y, Li S, Zhang D, He R. TUG1 knockdown ameliorates atherosclerosis via up-regulating the expression of miR-133a target gene FGF1. Cardiovasc Pathol. 2018;33: 6-15. doi: 10.1016/j.carpath.2017.11.004. https://doi.org/10.1016/j.carpath.2017.1...

	lncRNAs	Mechanism	Effect	References
Inflammatory response	ANRIL	TNF-α/NF-kB-ANRIL/YY1-IL6/8	⁺ (+) represents prompt or increase, and	³⁴34 Zhou X, Han X, Wittfeldt A, Sun J, Liu C, Wang X, et al. Long non-coding RNA ANRIL regulates inflammatory responses as a novel component of NF-κB pathway. RNA Biol. 2016;1(1):98-108. doi: 10.3892/mmr.2020.11203 https://doi.org/10.3892/mmr.2020.11203...
	MALAT1	MALAT1-p65/p50-TNF-α and IL-6	⁻ (−) represents prevent or decrease.	⁴⁰40 Zhao G, Su Z, Song D, Mao Y, Mao X. The long non-coding RNA MALAT1 regulates the lipopolysaccharide-induced inflammatory response through its interaction with NF-κB. FEBS Lett. 2016;590(17): 2884-95. doi: 10.1002/1873-3468.12315 https://doi.org/10.1002/1873-3468.12315...
	MALAT1	ceRNA (miR-503 or miR-155)	⁻ (−) represents prevent or decrease.	⁶¹61 Cremer S, Michalik KM, Fischer A,Jae N, Winter C. Hematopoietic Deficiency of the Long Non-coding RNA MALAT1 Promotes Atherosclerosis and Plaque Inflammation. Circulation. 2019;139(10):1320-34. doi: 10.1016/j.febslet.2015.08.046. https://doi.org/10.1016/j.febslet.2015.0... ,⁶²62 Li S, Sun Y, Zhong L, Xiao Z, Yang M, Chen M, et al. The suppression of ox-LDL-induced inflammatory cytokine release and apoptosis of HCAECs by long non-coding RNA-MALAT1 via regulating microRNA-155/SOCS1 pathway. Nutr Metabol Cardiovasc Dis. 2018; 28(11): 1175-87. . doi: 10.1016/j.numecd.2018.06.017. https://doi.org/10.1016/j.numecd.2018.06...
	H19	ceRNA (miR-130b)	⁻ (−) represents prevent or decrease.
	NEAT1	ceRNA (miR-342-3p)	⁺ (+) represents prompt or increase, and	⁷⁰70 Wang L, Xia JW, Ke ZP, Zhang H. Blockade of NEAT1 represses inflammation response and lipid uptake via modulating miR-342-3p in human macrophages THP-1 cells. J Cell Physiol.2019;234(4): 5319-26. doi: 10.1002/jcp.27340. https://doi.org/10.1002/jcp.27340...
	TUG1	ceRNA (miR-133a)	⁺ (+) represents prompt or increase, and	⁷²72 Zhang L, Cheng H, Yue Y, Li S, Zhang D, He R. TUG1 knockdown ameliorates atherosclerosis via up-regulating the expression of miR-133a target gene FGF1. Cardiovasc Pathol. 2018;33: 6-15. doi: 10.1016/j.carpath.2017.11.004. https://doi.org/10.1016/j.carpath.2017.1...

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[1] Mailing Address: Yongqiang Li • The Third Affiliated Hospital of Southern Medical University – GuangDong GuangZhou 510000 – China. E-mail: liyongqiang851@163.com