Long noncoding RNA PVT1 contributes to vascular endothelial cell proliferation via inhibition of miR‑190a‑5p in diagnostic biomarker evaluation of chronic heart failure

Sun,Bin; Meng,Meng; Wei,Jiali; Wang,Shuguang

doi:10.3892/etm.2020.8599

Long noncoding RNA PVT1 contributes to vascular endothelial cell proliferation via inhibition of miR‑190a‑5p in diagnostic biomarker evaluation of chronic heart failure

Authors:
- Bin Sun
- Meng Meng
- Jiali Wei
- Shuguang Wang
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Affiliations: Department of Emergency, Yidu Central Hospital of Weifang, Weifang, Shandong 262500, P.R. China, Department of Cardiovascular Medicine, Yidu Central Hospital of Weifang, Weifang, Shandong 262500, P.R. China, Department of Cardiovascular Medicine, Weifang People's Hospital, Weifang, Shandong 261000, P.R. China
Published online on: March 12, 2020 https://doi.org/10.3892/etm.2020.8599
Pages: 3348-3354
Copyright: © Sun et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Long noncoding RNAs (lncRNAs) and microRNAs (miRs) serve critical roles in various cellular processes and can be used as noninvasive biomarkers in human diseases. The present study aimed to investigate the effects of lncRNA plasmacytoma variant translocation 1 (PVT1) and miR‑190a‑5p on vascular endothelial cell (EC) proliferation and assess their clinical value in the diagnosis of chronic heart failure (CHF). The expression of PVT1 and miR‑190a‑5p was investigated using reverse transcription‑quantitative PCR. The interaction between PVT1 and miR‑190a‑5p was confirmed using a luciferase reporter assay. A Cell Counting Kit‑8 assay was performed to examine EC proliferation. A receiver operating characteristic (ROC) curve was plotted to evaluate the diagnostic value of PVT1 and miR‑190a‑5p. PVT1 directly decreased the expression of miR‑190a‑5p in ECs. Overexpression of miR‑190a‑5p in ECs led to inhibited cell proliferation and miR‑190a‑5p antagonized the promotive effect of PVT1 on EC proliferation. Serum expression of PVT1 increased, while serum expression of miR‑190a‑5p decreased in patients with CHF compared with healthy controls (all P<0.001). The ROC curves indicated that PVT1 and miR‑190a‑5p were two diagnostic biomarkers of CHF, and the combination of PVT1 and miR‑190a‑5p showed better diagnostic accuracy compared with using PVT1 or miR‑190‑5p alone. In conclusion, the present study demonstrated that PVT1 promoted EC proliferation by directly suppressing miR‑190a‑5p. Circulating PVT1 and miR‑190a‑5p are possible two candidate diagnostic biomarkers of CHF, and the combined detection of the two indicators may provide a novel approach for CHF diagnosis.

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1	Tanai E and Frantz S: Pathophysiology of heart failure. Compr Physiol. 6:187–214. 2015.PubMed/NCBI View Article : Google Scholar
2	Hoffman TM: Chronic heart failure. Pediatr Crit Care Med. 17 (8 Suppl 1):S119–S123. 2016.
3	Ford I, Robertson M, Komajda M, Böhm M, Borer JS, Tavazzi L and Swedberg K: SHIFT Investigators: Top ten risk factors for morbidity and mortality in patients with chronic systolic heart failure and elevated heart rate: The SHIFT Risk Model. Int J Cardiol. 184:163–169. 2015.PubMed/NCBI View Article : Google Scholar
4	Maggioni AP: Epidemiology of heart failure in Europe. Heart Fail Clin. 11:625–635. 2015.PubMed/NCBI View Article : Google Scholar
5	Heil B and Tang WH: Biomarkers: Their potential in the diagnosis and treatment of heart failure. Cleve Clin J Med. 82 (12 Suppl 2):S28–S35. 2015.PubMed/NCBI View Article : Google Scholar
6	Schaub JA, Coca SG, Moledina DG, Gentry M, Testani JM and Parikh CR: Amino-Terminal Pro-B-type natriuretic peptide for diagnosis and prognosis in patients with renal dysfunction: A systematic review and meta-analysis. JACC Heart Fail. 3:977–989. 2015.PubMed/NCBI View Article : Google Scholar
7	He X, Ji J, Wang T, Wang MB and Chen XL: Upregulation of Circulating miR-195-3p in Heart Failure. Cardiology. 138:107–114. 2017.PubMed/NCBI View Article : Google Scholar
8	Eelen G, de Zeeuw P, Treps L, Harjes U, Wong BW and Carmeliet P: Endothelial cell metabolism. Physiol Rev. 98:3–58. 2018.PubMed/NCBI View Article : Google Scholar
9	Sieve I, Munster-Kuhnel AK and Hilfiker-Kleiner D: Regulation and function of endothelial glycocalyx layer in vascular diseases. Vascul Pharmacol. 100:26–33. 2018.PubMed/NCBI View Article : Google Scholar
10	Sager HB, Hulsmans M, Lavine KJ, Moreira MB, Heidt T, Courties G, Sun Y, Iwamoto Y, Tricot B, Khan OF, et al: Proliferation and recruitment contribute to myocardial macrophage expansion in chronic heart failure. Circ Res. 119:853–864. 2016.PubMed/NCBI View Article : Google Scholar
11	Uchida S and Dimmeler S: Long noncoding RNAs in cardiovascular diseases. Circ Res. 116:737–750. 2015.PubMed/NCBI View Article : Google Scholar
12	Kong Q and Qiu M: Long noncoding RNA SNHG15 promotes human breast cancer proliferation, migration and invasion by sponging miR-211-3p. Biochem Biophys Res Commun. 495:1594–1600. 2018.PubMed/NCBI View Article : Google Scholar
13	Dangwal S, Schimmel K, Foinquinos A, Xiao K and Thum T: Noncoding RNAs in heart failure. Handb Exp Pharmacol. 243:423–445. 2017.PubMed/NCBI View Article : Google Scholar
14	Kumarswamy R, Bauters C, Volkmann I, Maury F, Fetisch J, Holzmann A, Lemesle G, de Groote P, Pinet F and Thum T: Circulating long noncoding RNA, LIPCAR, predicts survival in patients with heart failure. Circ Res. 114:1569–1575. 2014.PubMed/NCBI View Article : Google Scholar
15	Yu YH, Hu ZY, Li MH, Li B, Wang ZM and Chen SL: Cardiac hypertrophy is positively regulated by long non-coding RNA PVT1. Int J Clin Exp Pathol. 8:2582–2589. 2015.PubMed/NCBI
16	Cao F, Li Z, Ding WM, Yan L and Zhao QY: LncRNA PVT1 regulates atrial fibrosis via miR-128-3p-SP1-TGF-β1-Smad axis in atrial fibrillation. Mol Med. 25(7)2019.PubMed/NCBI View Article : Google Scholar
17	Zheng J, Hu L, Cheng J, Xu J, Zhong Z, Yang Y and Yuan Z: lncRNA PVT1 promotes the angiogenesis of vascular endothelial cell by targeting miR26b to activate CTGF/ANGPT2. Int J Mol Med. 42:489–496. 2018.PubMed/NCBI View Article : Google Scholar
18	Qiu Z, Li H, Wang J and Sun C: MiR-146a and miR-146b in the diagnosis and prognosis of papillary thyroid carcinoma. Oncol Rep. 38:2735–2740. 2017.PubMed/NCBI View Article : Google Scholar
19	Zhao Y, Ponnusamy M, Zhang L, Zhang Y, Liu C, Yu W, Wang K and Li P: The role of miR-214 in cardiovascular diseases. Eur J Pharmacol. 816:138–145. 2017.PubMed/NCBI View Article : Google Scholar
20	Liu B, Li J and Cairns MJ: Identifying miRNAs, targets and functions. Brief Bioinform. 15:1–19. 2014.PubMed/NCBI View Article : Google Scholar
21	Zhao L, Han T, Li Y, Sun J, Zhang S, Liu Y, Shan B, Zheng D and Shi J: The lncRNA SNHG5/miR-32 axis regulates gastric cancer cell proliferation and migration by targeting KLF4. FASEB J. 31:893–903. 2017.PubMed/NCBI View Article : Google Scholar
22	Xue W, Chen J, Liu X, Gong W, Zheng J, Guo X, Liu Y, Liu L, Ma J, Wang P, et al: PVT1 regulates the malignant behaviors of human glioma cells by targeting miR-190a-5p and miR-488-3p. Biochim Biophys Acta Mol Basis Dis. 1864:1783–1794. 2018.PubMed/NCBI View Article : Google Scholar
23	Wong LL, Armugam A, Sepramaniam S, Karolina DS, Lim KY, Lim JY, Chong JP, Ng JY, Chen YT, Chan MM, et al: Circulating microRNAs in heart failure with reduced and preserved left ventricular ejection fraction. Eur J Heart Fail. 17:393–404. 2015.PubMed/NCBI View Article : Google Scholar
24	WRITING COMMITTEE MEMBERS, Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, et al: 2013 ACCF/AHA guideline for the management of heart failure: A report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines. Circulation 128: e240-e327, 2013.
25	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001.PubMed/NCBI View Article : Google Scholar
26	Aman J, Weijers EM, van Nieuw Amerongen GP, Malik AB and van Hinsbergh VW: Using cultured endothelial cells to study endothelial barrier dysfunction: Challenges and opportunities. Am J Physiol Lung Cell Mol Physiol. 311:L453–L466. 2016.PubMed/NCBI View Article : Google Scholar
27	Jufri NF, Mohamedali A, Avolio A and Baker MS: Mechanical stretch: Physiological and pathological implications for human vascular endothelial cells. Vascular Cell. 7(8)2015.PubMed/NCBI View Article : Google Scholar
28	Koyama T, Sakurai T, Kamiyoshi A, Ichikawa-Shindo Y, Kawate H and Shindo T: Adrenomedullin-RAMP2 system in vascular endothelial cells. J Atheroscler Thromb. 22:647–653. 2015.PubMed/NCBI View Article : Google Scholar
29	Franssen C, Chen S, Unger A, Korkmaz HI, De Keulenaer GW, Tschöpe C, Leite-Moreira AF, Musters R, Niessen HW, Linke WA, et al: Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC Heart Fail. 4:312–324. 2016.PubMed/NCBI View Article : Google Scholar
30	Zheng B, Yin WN, Suzuki T, Zhang XH, Zhang Y, Song LL, Jin LS, Zhan H, Zhang H, Li JS and Wen JK: Exosome-mediated miR-155 transfer from smooth muscle cells to endothelial cells induces endothelial injury and promotes atherosclerosis. Mol Ther. 25:1279–1294. 2017.PubMed/NCBI View Article : Google Scholar
31	Schober A, Nazari-Jahantigh M, Wei Y, Bidzhekov K, Gremse F, Grommes J, Megens RT, Heyll K, Noels H, Hristov M, et al: MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1. Nat Med. 20:368–376. 2014.PubMed/NCBI View Article : Google Scholar
32	Duan Q, Yang L, Gong W, Chaugai S, Wang F, Chen C, Wang P, Zou MH and Wang DW: MicroRNA-214 Is upregulated in heart failure patients and suppresses xbp1-mediated endothelial cells angiogenesis. J Cell Physiol. 230:1964–1973. 2015.PubMed/NCBI View Article : Google Scholar
33	Hill SA, Booth RA, Santaguida PL, Don-Wauchope A, Brown JA, Oremus M, Ali U, Bustamam A, Sohel N, McKelvie R, et al: Use of BNP and NT-proBNP for the diagnosis of heart failure in the emergency department: A systematic review of the evidence. Heart Fail Rev. 19:421–438. 2014.PubMed/NCBI View Article : Google Scholar
34	Liu T, Zhang X, Gao S, Jing F, Yang Y, Du L, Zheng G, Li P, Li C and Wang C: Exosomal long noncoding RNA CRNDE-h as a novel serum-based biomarker for diagnosis and prognosis of colorectal cancer. Oncotarget. 7:85551–85563. 2016.PubMed/NCBI View Article : Google Scholar
35	Gao L, Liu Y, Guo S, Yao R, Wu L, Xiao L, Wang Z, Liu Y and Zhang Y: Circulating long noncoding RNA HOTAIR is an essential mediator of acute myocardial infarction. Cell Physiol Biochem. 44:1497–1508. 2017.PubMed/NCBI View Article : Google Scholar
36	Xuan L, Sun L, Zhang Y, Huang Y, Hou Y, Li Q, Guo Y, Feng B, Cui L, Wang X, et al: Circulating long non-coding RNAs NRON and MHRT as novel predictive biomarkers of heart failure. J Cell Mol Med. 21:1803–1814. 2017.PubMed/NCBI View Article : Google Scholar