SNHG16 accelerates the proliferation of primary cardiomyocytes by targeting miRNA‑770‑5p

Yang,Linshan; Lu,Yan; Ming,Jie; Pan,Yuzhu; Yu,Renbin; Wu,Yuhui; Wang,Tao

doi:10.3892/etm.2020.9083

SNHG16 accelerates the proliferation of primary cardiomyocytes by targeting miRNA‑770‑5p

Authors:
- Linshan Yang
- Yan Lu
- Jie Ming
- Yuzhu Pan
- Renbin Yu
- Yuhui Wu
- Tao Wang
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Affiliations: Department of Cardiac Surgery, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266003, P.R. China, Department of Otorhinolaryngology, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266003, P.R. China, Department of Oncology, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266003, P.R. China
Published online on: July 29, 2020 https://doi.org/10.3892/etm.2020.9083
Pages: 3221-3227
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The present study aimed to clarify the influence of long non‑coding RNA small nuclear host gene 16 (lncRNA SNHG16) on cardiomyocyte proliferation following ischemia/reperfusion injury (IRI) and the potential mechanism. An IRI model in mice was established by performing ligation of the anterior descending coronary artery (LAD). Primary cardiomyocytes were isolated from newborn mice and subjected to H2O2 treatment to mimic in vitro IRI. Relative levels of SNHG16 and miRNA‑770‑5p in both in vivo and in vitro IRI models were examined. The regulatory effects of SNHG16 and miRNA‑770‑5p on the proliferative ability of H2O2‑treated cardiomyocytes were assessed by Cell Counting Kit‑8 (CCK‑8) and 5‑ethynyl‑2'‑deoxyuridine (EdU) assay. The binding relationship between SNHG16 and miRNA‑770‑5p was verified through dual‑luciferase reporter gene assay. It is found that SNHG16 was time‑dependently downregulated in the IRI models. Overexpression of SNHG16 enhanced the proliferative ability of the cardiomyocytes. miRNA‑770‑5p was found to be a direct target of SNHG16. Moreover, SNHG16 was able to negatively regulate the miRNA‑770‑5p level. Overexpression of miRNA‑770‑5p partially reversed the role of SNHG16 on accelerating cardiomyocyte proliferation. Collectively, SNHG16 accelerates the proliferative ability of cardiomyocytes following IRI by negatively regulating miRNA‑770‑5p.

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1	Hausenloy DJ and Yellon DM: Myocardial ischemia-reperfusion injury: A neglected therapeutic target. J Clin Invest. 123:92–100. 2013.PubMed/NCBI View Article : Google Scholar
2	Song XD, Feng JP and Yang RX: Alamandine protects rat from myocardial ischemia-reperfusion injury by activating JNK and inhibiting NF-KB. Eur Rev Med Pharmacol Sci. 23:6718–6726. 2019.PubMed/NCBI View Article : Google Scholar
3	Ibanez B, Heusch G, Ovize M and Van de Werf F: Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol. 65:1454–1471. 2015.PubMed/NCBI View Article : Google Scholar
4	Martindale JJ and Metzger JM: Uncoupling of increased cellular oxidative stress and myocardial ischemia reperfusion injury by directed sarcolemma stabilization. J Mol Cell Cardiol. 67:26–37. 2014.PubMed/NCBI View Article : Google Scholar
5	Li X, Wu Z, Fu X and Han W: Long noncoding RNAs: Insights from biological features and functions to diseases. Med Res Rev. 33:517–553. 2013.PubMed/NCBI View Article : Google Scholar
6	Schmitz SU, Grote P and Herrmann BG: Mechanisms of long noncoding RNA function in development and disease. Cell Mol Life Sci. 73:2491–2509. 2016.PubMed/NCBI View Article : Google Scholar
7	Dabek J, Owczarek A, Gasior Z, Ulczok R, Skowerski M, Kulach A, Mazurek U and Bochenek A: Oligonucleotide microarray analysis of genes regulating apoptosis in chronically ischemic and postinfarction myocardium. Biochem Genet. 46:241–247. 2008.PubMed/NCBI View Article : Google Scholar
8	Pitts KR, Derry JM, Kerkof K, Lawrence WA and Toombs CF: Differentially regulated functional gene clusters identified during ischemia and reperfusion in isolated cardiac myocytes using coverslip hypoxia. J Pharmacol Toxicol Methods. 57:42–51. 2008.PubMed/NCBI View Article : Google Scholar
9	Mercer TR and Mattick JS: Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol. 20:300–307. 2013.PubMed/NCBI View Article : Google Scholar
10	Small EM and Olson EN: Pervasive roles of microRNAs in cardiovascular biology. Nature. 469:336–342. 2011.PubMed/NCBI View Article : Google Scholar
11	Wu HJ, Tang GM, Shao PY, Zou HX, Shen WF, Huang MD, Pan HH, Zhai CL and Qian G: Long non-coding RNA NEAT1 modulates hypoxia/reoxygenation-induced cardiomyocyte injury via targeting microRNA-520a. Exp Ther Med. 18:2199–2206. 2019.PubMed/NCBI View Article : Google Scholar
12	Gong X, Zhu Y, Chang H, Li Y and Ma F: Long noncoding RNA MALAT1 promotes cardiomyocyte apoptosis after myocardial infarction via targeting miR-144-3p. Biosci Rep. 39(BSR20191103)2019.PubMed/NCBI View Article : Google Scholar
13	Du XJ, Wei J, Tian D, Yan C, Hu P, Wu X, Yang W and Hu X: NEAT1 promotes myocardial ischemia-reperfusion injury via activating the MAPK signaling pathway. J Cell Physiol. 234:18773–18780. 2019.PubMed/NCBI View Article : Google Scholar
14	Zhu C, Cheng D, Qiu X, Zhuang M and Liu Z: Long noncoding RNA SNHG16 promotes cell proliferation by sponging MicroRNA-205 and upregulating ZEB1 expression in osteosarcoma. Cell Physiol Biochem. 51:429–440. 2018.PubMed/NCBI View Article : Google Scholar
15	Feng F, Chen A, Huang J, Xia Q, Chen Y and Jin X: Long noncoding RNA SNHG16 contributes to the development of bladder cancer via regulating miR-98/STAT3/Wnt/β-catenin pathway axis. J Cell Biochem. 119:9408–9418. 2018.PubMed/NCBI View Article : Google Scholar
16	Han W, Du X, Liu M, Wang J, Sun L and Li Y: Increased expression of long non-coding RNA SNHG16 correlates with tumor progression and poor prognosis in non-small cell lung cancer. Int J Biol Macromol. 121:270–278. 2019.PubMed/NCBI View Article : Google Scholar
17	Yang BY, Meng Q, Sun Y, Gao L and Yang JX: Long non-coding RNA SNHG16 contributes to glioma malignancy by competitively binding miR-20a-5p with E2F1. J Biol Regul Homeost Agents. 32:251–261. 2018.PubMed/NCBI
18	Yang XS, Wang GX and Luo L: Long non-coding RNA SNHG16 promotes cell growth and metastasis in ovarian cancer. Eur Rev Med Pharmacol Sci. 22:616–622. 2018.PubMed/NCBI View Article : Google Scholar
19	Cai C, Huo Q, Wang X, Chen B and Yang Q: SNHG16 contributes to breast cancer cell migration by competitively binding miR-98 with E2F5. Biochem Biophys Res Commun. 485:272–278. 2017.PubMed/NCBI View Article : Google Scholar
20	Wang D, Lin B, Zhang W and Wang X: Up-regulation of SNHG16 induced by CTCF accelerates cardiac hypertrophy by targeting miR-182-5p/IGF1 axis. Call Biol Int, Mar 3, 2020 (Epub ahead of print).
21	An JH, Chen ZY, Ma QL, Wang HJ, Zhang JQ and Shi FW: LncRNA SNHG16 promoted proliferation and inflammatory response of macrophages through miR-17-5p/NF-κB signaling pathway in patients with atherosclerosis. Eur Rev Med Pharmacol Sci. 23:8665–8677. 2019.PubMed/NCBI View Article : Google Scholar
22	Goldenberg I, Shainberg A, Jacobson KA, Shneyvays V and Grossman E: Adenosine protects against angiotensin II-induced apoptosis in rat cardiocyte cultures. Mol Cell Biochem. 252:133–139. 2003.PubMed/NCBI View Article : Google Scholar
23	Chen J, Larsson L, Haugen E, Fedorkova O, Angwald E, Waagstein F and Fu M: Effects of autoantibodies removed by immunoadsorption from patients with dilated cardiomyopathy on neonatal rat cardiomyocytes. Eur J Heart Fail. 8:460–467. 2006.PubMed/NCBI View Article : Google Scholar
24	Pagidipati NJ and Gaziano TA: Estimating deaths from cardiovascular disease: A review of global methodologies of mortality measurement. Circulation. 127:749–756. 2013.PubMed/NCBI View Article : Google Scholar
25	Dong J, Zhao Y and He XK: Down-regulation of miR-192 protects against rat ischemia-reperfusion injury after myocardial infarction. Eur Rev Med Pharmacol Sci. 22:6109–6118. 2018.PubMed/NCBI View Article : Google Scholar
26	Wu H, Ye M, Yang J and Ding J: Modulating endoplasmic reticulum stress to alleviate myocardial ischemia and reperfusion injury from basic research to clinical practice: A long way to go. Int J Cardiol. 223:630–631. 2016.PubMed/NCBI View Article : Google Scholar
27	Wang K, Long B, Zhou LY, Liu F, Zhou QY, Liu CY, Fan YY and Li PF: CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat Commun. 5(3596)2014.PubMed/NCBI View Article : Google Scholar
28	Viereck J, Kumarswamy R, Foinquinos A, Xiao K, Avramopoulos P, Kunz M, Dittrich M, Maetzig T, Zimmer K, Remke J, et al: Long noncoding RNA Chast promotes cardiac remodeling. Sci Transl Med. 8(326ra22)2016.PubMed/NCBI View Article : Google Scholar
29	Wang K, Liu F, Liu CY, An T, Zhang J, Zhou LY, Wang M, Dong YH, Li N, Gao JN, et al: The long noncoding RNA NRF regulates programmed necrosis and myocardial injury during ischemia and reperfusion by targeting miR-873. Cell Death Differ. 23:1394–1405. 2016.PubMed/NCBI View Article : Google Scholar
30	Liu Y, Zhou D, Li G, Ming X, Tu YF, Tian J, Lu H and Yu B: Long non coding RNA-UCA1 contributes to cardiomyocyte apoptosis by suppression of p27 expression. Cell Physiol Biochem. 35:1986–1998. 2015.PubMed/NCBI View Article : Google Scholar
31	Ulitsky I: Interactions between short and long noncoding RNAs. FEBS Lett. 592:2874–2883. 2018.PubMed/NCBI View Article : Google Scholar
32	Chan JJ and Tay Y: Noncoding RNA: RNA regulatory networks in cancer. Int J Mol Sci. 19(1310)2018.PubMed/NCBI View Article : Google Scholar
33	Tay Y, Rinn J and Pandolfi PP: The multilayered complexity of ceRNA crosstalk and competition. Nature. 505:344–352. 2014.PubMed/NCBI View Article : Google Scholar
34	Kartha RV and Subramanian S: Competing endogenous RNAs (ceRNAs): New entrants to the intricacies of gene regulation. Front Genet. 5(8)2014.PubMed/NCBI View Article : Google Scholar
35	Karreth FA and Pandolfi PP: ceRNA cross-talk in cancer: When ce-bling rivalries go awry. Cancer Discov. 3:1113–1121. 2013.PubMed/NCBI View Article : Google Scholar
36	Liu S, Zhang W, Liu K and Liu Y: LncRNA SNHG16 promotes tumor growth of pancreatic cancer by targeting miR-218-5p. Biomed Pharmacother. 114(108862)2019.PubMed/NCBI View Article : Google Scholar