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General Thoracic and Cardiovascular Surgery

Published in:

07-04-2022 | Arterial Diseases | Original Article

Circular RNA circ_0001445 alleviates the ox-LDL-induced endothelial injury in human primary aortic endothelial cells through regulating ABCG1 via acting as a sponge of miR-208b-5p

Authors: Zhihua Yang, Xing Liang, Lixia Yang

Published in: General Thoracic and Cardiovascular Surgery | Issue 9/2022

Abstract

Background

Coronary artery disease (CAD) originates from the blockage of the inner walls of the coronary arteries due to a plaque buildup. Circular RNA (circRNA) circ_0001445 has been reported to be downregulated in patients with a higher coronary atherosclerotic burden. This study is designed to explore the role and mechanism of circ_0001445 on the oxidized low-density lipoprotein (ox-LDL)-induced endothelial cell damage.

Methods

Circ_0001445, microRNA-208b-5p (miR-208b-5p), and ATP-binding cassette sub-family G member 1 (ABCG1) levels were detected by real-time quantitative polymerase chain reaction (RT-qPCR). Inflammatory cytokines levels, cell viability, proliferation, migration were detected by Enzyme-linked immunosorbent assay (ELISA) kits, Cell Counting Kit-8 (CCK-8), 5-ethynyl-2’-deoxyuridine (EdU), and transwell assays, respectively. Protein levels were determined by western blot assay. The binding between miR-208b-5p and circ_0001445 or ABCG1 was predicted by circBank or TargetScan, and then verified by a dual-luciferase reporter, RNA Immunoprecipitation (RIP), and RNA pull-down assays.

Results

Circ_0001445 and ABCG1 were decreased, and miR-208b-5p was increased in CAD patients and ox-LDL-treated HAECs. Also, circ_0001445 overexpression could weaken ox-LDL-triggered HAEC injury by boosting proliferation, migration, and repressing inflammation and extracellular matrix (ECM). Mechanically, circ_0001445 directly targeted miR-208b-5p. Furthermore, miR-208b-5p mediated the modulation of circ_0001445 in ox-LDL-induced HAEC injury. ABCG1 acted as a direct target of miR-208b-5p, and the downregulation of miR-208b-5p relieved ox-LDL-induced HAEC damage by interacting with ABCG1. Additionally, circ_0001445 regulated ABCG1 expression by sponging miR-208b-5p.

Conclusion

Circ_0001445 could abate ox-LDL-mediated HAEC damage by the miR-208b-5p/ABCG1 axis, providing a novel insight into the pathogenesis and treatment of CAD.

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Malakar AK, Choudhury D, Halder B, et al. A review on coronary artery disease, its risk factors, and therapeutics. J Cell Physiol. 2019;234(10):16812–23. https://doi.org/10.1002/jcp.28350.CrossRefPubMed

McCullough PA. Coronary artery disease. Clin J Am Soc Nephrol. 2007;2(3):611–6. https://doi.org/10.2215/cjn.03871106.CrossRefPubMed

Li X, Wu C, Lu J, et al. Cardiovascular risk factors in China: a nationwide population-based cohort study. Lancet Public Health. 2020;5(12):e672–81. https://doi.org/10.1016/s2468-2667(20)30191-2.CrossRefPubMed

Liu L. Cardiovascular diseases in China. Biochem Cell Biol. 2007;85(2):157–63. https://doi.org/10.1139/o07-004.CrossRefPubMed

Bentzon JF, Otsuka F, Virmani R, et al. Mechanisms of plaque formation and rupture. Circ Res. 2014;114(12):1852–66. https://doi.org/10.1161/circresaha.114.302721.CrossRefPubMed

Ishida M, Sakuma H. Magnetic resonance of coronary arteries: assessment of luminal narrowing and blood flow in the coronary arteries. J Thorac Imaging. 2014;29(3):155–62. https://doi.org/10.1097/rti.0000000000000081.CrossRefPubMed

Maiolino G, Rossitto G, Caielli P, et al. The role of oxidized low-density lipoproteins in atherosclerosis: the myths and the facts. Mediators Inflamm. 2013. https://doi.org/10.1155/2013/714653.CrossRefPubMedPubMedCentral

Yang H, Mohamed AS, Zhou SH. Oxidized low density lipoprotein, stem cells, and atherosclerosis. Lipids Health Dis. 2012;11:85. https://doi.org/10.1186/1476-511x-11-85.CrossRefPubMedPubMedCentral

Zhao X, Zhang HW, Sun D, et al. Relation of oxidized-low-density lipoprotein and high-density lipoprotein subfractions in non-treated patients with coronary artery disease. Prostaglandins Other Lipid Mediat. 2019;144: 106345. https://doi.org/10.1016/j.prostaglandins.2019.106345.CrossRefPubMed

10.

Zhang YH, He K, Shi G. Effects of microRNA-499 on the inflammatory damage of endothelial cells during coronary artery disease via the targeting of PDCD4 through the NF-Κβ/TNF-α signaling pathway. Cell Physiol Biochem. 2017;44(1):110–24. https://doi.org/10.1159/000484588.CrossRefPubMed

11.

Zhang C, Ge S, Gong W, et al. LncRNA ANRIL acts as a modular scaffold of WDR5 and HDAC3 complexes and promotes alteration of the vascular smooth muscle cell phenotype. Cell Death Dis. 2020;11(6):435. https://doi.org/10.1038/s41419-020-2645-3.CrossRefPubMedPubMedCentral

12.

Peng Y, Calin GA. Crucial role of non-coding RNAs in disease. Cancer Lett. 2018. https://doi.org/10.1016/j.canlet.2018.02.001.CrossRefPubMedPubMedCentral

13.

Santosh B, Varshney A, Yadava PK. Non-coding RNAs: biological functions and applications. Cell Biochem Funct. 2015;33(1):14–22. https://doi.org/10.1002/cbf.3079.CrossRefPubMed

14.

Birney E, Stamatoyannopoulos JA, Dutta A, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447(7146):799–816. https://doi.org/10.1038/nature05874.CrossRefPubMed

15.

Kristensen LS, Andersen MS, Stagsted LVW, et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20(11):675–91. https://doi.org/10.1038/s41576-019-0158-7.CrossRefPubMed

16.

Barrett SP, Wang PL, Salzman J. Circular RNA biogenesis can proceed through an exon-containing lariat precursor. Elife. 2015;4: e07540. https://doi.org/10.7554/eLife.07540.CrossRefPubMedPubMedCentral

17.

Patop IL, Wüst S, Kadener S. Past, present, and future of circRNAs. Embo J. 2019;38(16):e100836. https://doi.org/10.1525/embj.2018100836.CrossRefPubMedPubMedCentral

18.

Han B, Chao J, Yao H. Circular RNA and its mechanisms in disease: From the bench to the clinic. Pharm Ther. 2018;187:31–44. https://doi.org/10.1016/j.pharmthera.2018.01.010.CrossRef

19.

Altesha MA, Ni T, Khan A, et al. Circular RNA in cardiovascular disease. J Cell Physiol. 2019;234(5):5588–600. https://doi.org/10.1002/jcp.27384.CrossRefPubMed

20.

Pan RY, Zhao CH, Yuan JX, et al. Circular RNA profile in coronary artery disease. Am J Transl Res. 2019;11(11):7115–25.PubMedPubMedCentral

21.

Wang L, Shen C, Wang Y, et al. Identification of circular RNA Hsa_circ_0001879 and Hsa_circ_0004104 as novel biomarkers for coronary artery disease. Atherosclerosis. 2019;286:88–96. https://doi.org/10.1016/j.atherosclerosis.2019.05.006.CrossRefPubMed

22.

Gao Y, Li G, Fan S, et al. Circ_0093887 upregulates CCND2 and SUCNR1 to inhibit the ox-LDL-induced endothelial dysfunction in atherosclerosis by functioning as a miR-876–3p sponge. Clin Exp Pharm Physiol. 2021. https://doi.org/10.1111/1440-1681.13504.CrossRef

23.

Vilades D, Martínez-Camblor P, Ferrero-Gregori A, et al. Plasma circular RNA hsa_circ_0001445 and coronary artery disease: performance as a biomarker. Faseb j. 2020;34(3):4403–14. https://doi.org/10.1096/fj.201902507R.CrossRefPubMed

24.

Cai Y, Xu L, Xu C, et al. Hsa_circ_0001445 inhibits ox-LDL-induced HUVECs inflammation, oxidative stress and apoptosis by regulating miRNA-640. Perfusion. 2020. https://doi.org/10.1177/0267659120979472.CrossRefPubMed

25.

Su Q, Lv X. Revealing new landscape of cardiovascular disease through circular RNA-miRNA-mRNA axis. Genomics. 2020;112(2):1680–5. https://doi.org/10.1016/j.ygeno.2019.10.006.CrossRefPubMed

26.

Panda AC. Circular RNAs Act as miRNA Sponges. Adv Exp Med Biol. 2018;1087:67–79. https://doi.org/10.1007/978-981-13-1426-1_6.CrossRefPubMed

27.

Hansen TB, Jensen TI, Clausen BH, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495(7441):384–8. https://doi.org/10.1038/nature11993.CrossRefPubMed

28.

Wang W, Li T, Gao L, et al. Plasma miR-208b and miR-499: potential biomarkers for severity of coronary artery disease. Dis Mark. 2019. https://doi.org/10.1155/2019/9842427.CrossRef

29.

Zhou Q, Schötterl S, Backes D, et al. Inhibition of miR-208b improves cardiac function in titin-based dilated cardiomyopathy. Int J Cardiol. 2017;230:634–41. https://doi.org/10.1016/j.ijcard.2016.12.171.CrossRefPubMed

30.

López-Jiménez E, Rojas AM, Andrés-León E. RNA sequencing and prediction tools for circular RNAs analysis. Adv Exp Med Biol. 2018;1087:17–33. https://doi.org/10.1007/978-981-13-1426-1_2.CrossRefPubMed

31.

Sekar S, Geiger P, Cuyugan L, et al. Identification of circular RNAs using RNA sequencing. J Vis Exp. 2019. https://doi.org/10.3791/59981.CrossRefPubMed

32.

Santer L, Bär C, Thum T. Circular RNAs: a novel class of functional RNA molecules with a therapeutic perspective. Mol Ther. 2019;27(8):1350–63. https://doi.org/10.1016/j.ymthe.2019.07.001.CrossRefPubMedPubMedCentral

33.

Ojha R, Nandani R, Chatterjee N, et al. Emerging role of circular RNAs as potential biomarkers for the diagnosis of human diseases. Adv Exp Med Biol. 2018;1087:141–57. https://doi.org/10.1007/978-981-13-1426-1_12.CrossRefPubMed

34.

Zhang S, Wang W, Wu X, et al. Regulatory roles of circular rnas in coronary artery disease. Mol Ther Nucleic Acids. 2020. https://doi.org/10.1016/j.omtn.2020.05.024.CrossRefPubMedPubMedCentral

35.

Bach LA. Endothelial cells and the IGF system. J Mol Endocrinol. 2015;54(1):R1-13. https://doi.org/10.1530/jme-14-0215.CrossRefPubMed

36.

Suna G, Wojakowski W, Lynch M, et al. Extracellular matrix proteomics reveals interplay of aggrecan and aggrecanases in vascular remodeling of stented coronary arteries. Circulation. 2018;137(2):166–83. https://doi.org/10.1161/circulationaha.116.023381.CrossRefPubMedPubMedCentral

37.

Nielsen SH, Mygind ND, Michelsen MM, et al. Accelerated collagen turnover in women with angina pectoris without obstructive coronary artery disease: an iPOWER substudy. Eur J Prev Cardiol. 2018;25(7):719–27. https://doi.org/10.1177/2047487318758750.CrossRefPubMed

38.

Tay Y, Rinn J, Pandolfi PP. The multilayered complexity of ceRNA crosstalk and competition. Nature. 2014;505(7483):344–52. https://doi.org/10.1038/nature12986.CrossRefPubMedPubMedCentral

39.

Corsten MF, Dennert R, Jochems S, et al. Circulating microRNA-208b and microRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet. 2010;3(6):499–506. https://doi.org/10.1161/circgenetics.110.957415.CrossRefPubMed

40.

Liu X, Yuan L, Chen F, et al. Circulating miR-208b: a potentially sensitive and reliable biomarker for the diagnosis and prognosis of acute myocardial infarction. Clin Lab. 2017;63(1):101–9. https://doi.org/10.7754/Clin.Lab.2016.160632.CrossRefPubMed

41.

Goldberg L, Tirosh-Wagner T, Vardi A, et al. Circulating microRNAs: a potential biomarker for cardiac damage, inflammatory response, and left ventricular function recovery in pediatric viral myocarditis. J Cardiovasc Transl Res. 2018;11(4):319–28. https://doi.org/10.1007/s12265-018-9814-0.CrossRefPubMed

42.

Pandzic E, Gelissen IC, Whan R, et al. The ATP binding cassette transporter, ABCG1, localizes to cortical actin filaments. Sci Rep. 2017. https://doi.org/10.1038/srep42025.CrossRefPubMedPubMedCentral

43.

Hutchins PM, Heinecke JW. Cholesterol efflux capacity, macrophage reverse cholesterol transport and cardioprotective HDL. Curr Opin Lipidol. 2015;26(5):388–93. https://doi.org/10.1097/mol.0000000000000209.CrossRefPubMedPubMedCentral

44.

Rafiei A, Ferns GA, Ahmadi R, et al. Expression levels of miR-27a, miR-329, ABCA1, and ABCG1 genes in peripheral blood mononuclear cells and their correlation with serum levels of oxidative stress and hs-CRP in the patients with coronary artery disease. IUBMB Life. 2021;73(1):223–37. https://doi.org/10.1002/iub.2421.CrossRefPubMed

45.

Rosenson RS, Brewer HB Jr, Ansell BJ, et al. Dysfunctional HDL and atherosclerotic cardiovascular disease. Nat Rev Cardiol. 2016;13(1):48–60. https://doi.org/10.1038/nrcardio.2015.124.CrossRefPubMed

Title: Circular RNA circ_0001445 alleviates the ox-LDL-induced endothelial injury in human primary aortic endothelial cells through regulating ABCG1 via acting as a sponge of miR-208b-5p
Authors: Zhihua Yang
Xing Liang
Lixia Yang
Publication date: 07-04-2022
Publisher: Springer Nature Singapore
Keyword: Arterial Diseases
Published in: General Thoracic and Cardiovascular Surgery / Issue 9/2022
Print ISSN: 1863-6705
Electronic ISSN: 1863-6713
DOI: https://doi.org/10.1007/s11748-022-01799-2

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Circular RNA circ_0001445 alleviates the ox-LDL-induced endothelial injury in human primary aortic endothelial cells through regulating ABCG1 via acting as a sponge of miR-208b-5p

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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