MicroRNA‑144 attenuates cardiac ischemia/reperfusion injury by targeting FOXO1 Corrigendum in /10.3892/etm.2020.8424

E,Lusha; Jiang,Hong; Lu,Zhibing

doi:10.3892/etm.2019.7161

MicroRNA‑144 attenuates cardiac ischemia/reperfusion injury by targeting FOXO1

Corrigendum in: /10.3892/etm.2020.8424

Authors:
- Lusha E
- Hong Jiang
- Zhibing Lu
View Affiliations

Affiliations: Department of Cardiology, Renmin Hospital of Wuhan University, Hubei General Hospital, Wuchang, Wuhan, Hubei 430060, P.R. China
Published online on: January 9, 2019 https://doi.org/10.3892/etm.2019.7161
Pages: 2152-2160
Copyright: © E et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Cardiovascular ischemic disease refers to a large class of conditions that are harmful to human health. A number of previous studies have demonstrated that microRNAs (miRs) have notable roles in regulating cardiac injury. miR‑144 is influential in the differentiation, growth, and metastatic processes of cells; however, the impact of miR‑144 in cardiac ischemia/reperfusion (I/R) injury has not been thoroughly elucidated to date. In the present study, reverse transcription quantitative polymerase chain reaction was used to evaluate RNA expression. In addition, TTC staining was performed to detect the infarct area of the ischemic myocardia and a terminal deoxynucleotidyl‑transferase‑mediated dUTP nick end labeling assay was utilized to detect the apoptosis of the myocardia. It was observed that miR‑144 expression is downregulated in an I/R model in rats and that overexpression of miR‑144 significantly reduced myocardial ischemic injury and apoptosis. Consistent with this result, similar findings were demonstrated in H9c2 cells subjected to hypoxia/reoxygenation. Bioinformatic analysis using MiRanda and TargetScan, and luciferase assays confirmed that forkhead box protein O1was the target of miR‑144. These findings suggest that miR‑144 may be exploited as a novel molecular marker or therapeutic target for myocardial I/R injury.

View Figures

View References

1	Carden DL and Granger DN: Pathophysiology of ischaemia-reperfusion injury. J Pathol. 190:255–266. 2000. View Article : Google Scholar : PubMed/NCBI
2	Dorweiler B, Pruefer D, Andrasi TB, Maksan SM, Schmiedt W, Neufang A and Vahl CF: Ischemia-reperfusion injury: Pathophysiology and clinical implications. Eur J Trauma Emerg Surg. 33:600–612. 2007. View Article : Google Scholar : PubMed/NCBI
3	Wang JX, Zhang XJ, Li Q, Wang K, Wang Y, Jiao JQ, Feng C, Teng S, Zhou LY, Gong Y, et al: MicroRNA-103/107 regulate programmed necrosis and myocardial ischemia/reperfusion injury through targeting FADD. Circ Res. 117:352–363. 2015. View Article : Google Scholar : PubMed/NCBI
4	Li Y, Wen S, Yao X, Liu W, Shen J, Deng W, Tang J, Li C and Liu K: MicroRNA-378 protects against intestinal ischemia/reperfusion injury via a mechanism involving the inhibition of intestinal mucosal cell apoptosis. Cell Death Dis. 8:e31272017. View Article : Google Scholar : PubMed/NCBI
5	Kang B, Li W, Xi W, Yi Y, Ciren Y, Shen H, Zhang Y, Jiang H, Xiao J and Wang Z: Hydrogen sulfide protects cardiomyocytes against apoptosis in ischemia/reperfusion through MiR-1-regulated histone deacetylase 4 pathway. Cell Physiol Biochem. 41:10–21. 2017. View Article : Google Scholar : PubMed/NCBI
6	Hausenloy DJ and Yellon DM: Myocardial ischemia-reperfusion injury: A neglected therapeutic target. J Clin Invest. 123:92–100. 2013. View Article : Google Scholar : PubMed/NCBI
7	Rakotovao A, Tanguy S, Toufektsian MC, Berthonneche C, Ducros V, Tosaki A, de Leiris J and Boucher F: Selenium status as determinant of connexin-43 dephosphorylation in ex vivo ischemic/reperfused rat myocardium. J Trace Elem Med Biol. 19:43–47. 2005. View Article : Google Scholar : PubMed/NCBI
8	Barandier C, Tanguy S, Pucheu S, Boucher F and De Leiris J: Effect of antioxidant trace elements on the response of cardiac tissue to oxidative stress. Ann N Y Acad Sci. 874:138–155. 1999. View Article : Google Scholar : PubMed/NCBI
9	Valinezhad Orang A, Safaralizadeh R and Kazemzadeh-Bavili M: Mechanisms of miRNA-mediated gene regulation from common downregulation to mRNA-specific upregulation. Int J Genomics. 2014:9706072014. View Article : Google Scholar : PubMed/NCBI
10	Bier A, Giladi N, Kronfeld N, Lee HK, Cazacu S, Finniss S, Xiang C, Poisson L, deCarvalho AC, Slavin S, et al: MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1. Oncotarget. 4:665–676. 2013. View Article : Google Scholar : PubMed/NCBI
11	Yang WB, Chen PH, Hsu T I, Fu TF, Su WC, Liaw H, Chang WC and Hung JJ: Sp1-mediated microRNA-182 expression regulates lung cancer progression. Oncotarget. 5:740–753. 2014. View Article : Google Scholar : PubMed/NCBI
12	Holik AK, Lieder B, Kretschy N, Somoza MM, Held S and Somoza V: N(ε)-Carboxymethyllysine increases the expression of miR-103/143 and enhances lipid accumulation in 3T3-L1 cells. J Cell Biochem. 117:2413–2422. 2016. View Article : Google Scholar : PubMed/NCBI
13	Di YF, Li DC, Shen YQ, Wang CL, Zhang DY, Shang AQ and Hu T: MiR-146b protects cardiomyocytes injury in myocardial ischemia/reperfusion by targeting Smad4. Am J Transl Res. 9:656–663. 2017.PubMed/NCBI
14	Ke ZP, Xu P, Shi Y and Gao AM: MicroRNA-93 inhibits ischemia-reperfusion induced cardiomyocyte apoptosis by targeting PTEN. Oncotarget. 7:28796–28805. 2016. View Article : Google Scholar : PubMed/NCBI
15	Wang K, Zhou LY, Wang JX, Wang Y, Sun T, Zhao B, Yang YJ, An T, Long B, Li N, et al: E2F1-dependent miR-421 regulates mitochondrial fragmentation and myocardial infarction by targeting Pink1. Nat Commun. 6:76192015. View Article : Google Scholar : PubMed/NCBI
16	Wang S, Xu Z and Wang L: Shuanghuang Shengbai granule cures myelosuppression and suppresses lung cancer progression: Mechanism and therapeutic targets from the aspect of microRNAs. Oncotarget. 8:62154–62166. 2017.PubMed/NCBI
17	Manikandan M, Deva Magendhra Rao AK, Arunkumar G, Manickavasagam M, Rajkumar KS, Rajaraman R and Munirajan AK: Oral squamous cell carcinoma: microRNA expression profiling and integrative analyses for elucidation of tumourigenesis mechanism. Mol Cancer. 15:282016. View Article : Google Scholar : PubMed/NCBI
18	Madhavan D, Peng C, Wallwiener M, Zucknick M, Nees J, Schott S, Rudolph A, Riethdorf S, Trumpp A, Pantel K, et al: Circulating miRNAs with prognostic value in metastatic breast cancer and for early detection of metastasis. Carcinogenesis. 37:461–470. 2016. View Article : Google Scholar : PubMed/NCBI
19	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-tie quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
20	Li J, Rohailla S, Gelber N, Rutka J, Sabah N, Gladstone RA, Wei C, Hu P, Kharbanda RK and Redington AN: MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol. 109:4232014. View Article : Google Scholar : PubMed/NCBI
21	Zhang X, Wang X, Zhu H, Zhu C, Wang Y, Pu WT, Jegga AG and Fan GC: Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J Mol Cell Cardiol. 49:841–850. 2010. View Article : Google Scholar : PubMed/NCBI
22	Huang Z, Ye B, Dai Z, Wu X, Lu Z, Shan P and Huang W: Curcumin inhibits autophagy and apoptosis in hypoxia/reoxygenation-induced myocytes. Mol Med Rep. 11:4678–4684. 2015. View Article : Google Scholar : PubMed/NCBI
23	Yin Y, Guan Y, Duan J, Wei G, Zhu Y, Quan W, Guo C, Zhou D, Wang Y, Xi M and Wen A: Cardioprotective effect of Danshensu against myocardial ischemia/reperfusion injury and inhibits apoptosis of H9c2 cardiomyocytes via Akt and ERK1/2 phosphorylation. Eur J Pharmacol. 699:219–226. 2013. View Article : Google Scholar : PubMed/NCBI
24	Hadi NR, Yusif FG, Yousif M and Jaen KK: Both castration and goserelin acetate ameliorate myocardial ischemia reperfusion injury and apoptosis in male rats. ISRN Pharmacol. 2014:2069512014. View Article : Google Scholar : PubMed/NCBI
25	Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM and Lieschke GJ: miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood. 113:1794–1804. 2009. View Article : Google Scholar : PubMed/NCBI
26	Sangokoya C, Telen MJ and Chi JT: microRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease. Blood. 116:4338–4348. 2010. View Article : Google Scholar : PubMed/NCBI
27	Puthanveetil P, Wan A and Rodrigues B: FoxO1 is crucial for sustaining cardiomyocyte metabolism and cell survival. Cardiovasc Res. 97:393–403. 2013. View Article : Google Scholar : PubMed/NCBI
28	Hosaka T, Biggs WR III, Tieu D, Boyer AD, Varki NM, Cavenee WK and Arden KC: Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA. 101:2975–2980. 2004. View Article : Google Scholar : PubMed/NCBI
29	Puthanveetil P, Wang Y, Zhang D, Wang F, Kim MS, Innis S, Pulinilkunnil T, Abrahani A and Rodrigues B: Cardiac triglyceride accumulation following acute lipid excess occurs through activation of a FoxO1-iNOS-CD36 pathway. Free Radic Biol Med. 51:352–363. 2011. View Article : Google Scholar : PubMed/NCBI
30	Puthanveetil P, Zhang D, Wang Y, Wang F, Wan A, Abrahani A and Rodrigues B: Diabetes triggers a PARP1 mediated death pathway in the heart through participation of FoxO1. J Mol Cell Cardiol. 53:677–686. 2012. View Article : Google Scholar : PubMed/NCBI
31	Chen CJ, Yu W, Fu YC, Wang X, Li JL and Wang W: Resveratrol protects cardiomyocytes from hypoxia-induced apoptosis through the SIRT1-FoxO1 pathway. Biochem Biophys Res Commun. 378:389–393. 2009. View Article : Google Scholar : PubMed/NCBI
32	Xu H, Zhu J, Hu C, Song H and Li Y: Inhibition of microRNA-181a may suppress proliferation and invasion and promote apoptosis of cervical cancer cells through the PTEN/Akt/FOXO1 pathway. J Physiol Biochem. 72:721–732. 2016. View Article : Google Scholar : PubMed/NCBI
33	Zhao M, Luo R, Liu Y, Gao L, Fu Z, Fu Q, Luo X, Chen Y, Deng X, Liang Z, et al: miR-3188 regulates nasopharyngeal carcinoma proliferation and chemosensitivity through a FOXO1-modulated positive feedback loop with mTOR-p-PI3K/AKT-c-JUN. Nat Commun. 7:113092016. View Article : Google Scholar : PubMed/NCBI
34	Yan C, Chen J, Li M, Xuan W, Su D, You H, Huang Y, Chen N and Liang X: A decrease in hepatic microRNA-9 expression impairs gluconeogenesis by targeting FOXO1 in obese mice. Diabetologia. 59:1524–1532. 2016. View Article : Google Scholar : PubMed/NCBI
35	Hou L, Chen J, Zheng Y and Wu C: Critical role of miR-155/FoxO1/ROS axis in the regulation of non-small cell lung carcinomas. Tumour Biol. 37:5185–5192. 2016. View Article : Google Scholar : PubMed/NCBI