Generic placeholder image

Current Medicinal Chemistry

Author(s): Xinyong Cai, Ping Zhang, Yong Yang, Yunxia Wang, Hongmin Zhu, Bin Li, Hong Zeng, Lang Hong and Liang Shao*

DOI: 10.2174/0929867329666220801162756

DownloadDownload PDF Flyer Cite As
MiR-30a-5p Promotes Vein Graft Restenosis by Inhibiting Cell Autophagy through Targeting ATG5

Page: [757 - 774] Pages: 18

  • * (Excluding Mailing and Handling)

Abstract

Objective: The aim of the study was to investigate the role of miR-30a-5p in restenosis of rats following vein grafting and the underlying mechanism.

Methods: Vein graft rat models were established and perfused with miR-30a-5p antagomir and si-ATG5 to probe the regulation of miR-30a-5p/ATG5 on intimal hyperplasia. Human saphenous vein smooth muscle cells (HSVSMCs) were obtained from the great saphenous veins of patients undergoing coronary artery bypass grafting and subjected to assays for autophagy, proliferation, and migration after gain and loss of function of miR-30a-5p and/or ATG5. The binding of miR-30a-5p and ATG5 was confirmed by RIP and dual-luciferase reporter assays.

Results: MiR-30a-5p expression gradually increased, ATG5 expression gradually decreased, and the intima was increasingly thickened during restenosis of grafted veins. Knockdown of miR-30a-5p in rats repressed the restenosis of vein grafts, while a deficiency of ATG5 reversed the effect of miR-30a-5p inhibition. Upregulation of miR-30a-5p enhanced the proliferation and migration of HSVSMCs and inhibited the autophagy, while downregulation of miR-30a-5p or overexpression of ATG5 showed opposite effects. ATG5 is a target gene of miR-30a-5p.

Conclusion: MiR-30a-5p exacerbates vein graft restenosis by repressing ATG5 expression and inhibiting autophagy.

Keywords: ein graft, Restenosis, MicroRNA-30a-5p, ATG5, Autophagy, Intimal hyperplasia

[1]
Lamy, A.; Devereaux, P.J.; Prabhakaran, D.; Taggart, D.P.; Hu, S.; Straka, Z.; Piegas, L.S.; Avezum, A.; Akar, A.R.; Lanas Zanetti, F.; Jain, A.R.; Noiseux, N.; Padmanabhan, C.; Bahamondes, J.C.; Novick, R.J.; Tao, L.; Olavegogeascoechea, P.A.; Airan, B.; Sulling, T.A.; Whitlock, R.P.; Ou, Y.; Gao, P.; Pettit, S.; Yusuf, S.; Investigators, C. Five-year outcomes after off-pump or on-pump coronary-artery bypass grafting. N. Engl. J. Med., 2016, 375(24), 2359-2368.
[http://dx.doi.org/10.1056/NEJMoa1601564] [PMID: 27771985]
[2]
Serruys, P.W.; Morice, M.C.; Kappetein, A.P.; Colombo, A.; Holmes, D.R.; Mack, M.J.; Ståhle, E.; Feldman, T.E.; van den Brand, M.; Bass, E.J.; Van Dyck, N.; Leadley, K.; Dawkins, K.D.; Mohr, F.W.; Investigators, S. Percutaneous coronary intervention versus coronary-artery bypass grafting for severe coronary artery disease. N. Engl. J. Med., 2009, 360(10), 961-972.
[http://dx.doi.org/10.1056/NEJMoa0804626] [PMID: 19228612]
[3]
Lopes, F.C.; Oliveira, O.W.B.; Moreira, D.G.; Santos, M.A.D.; Oliveira, J.L.R.; Cruz, C.B.; Lubanco Filho, G.; Chaccur, P.; Souza, L.C.B. Use of doppler ultrasound for saphenous vein mapping to obtain grafts for coronary artery bypass grafting. Rev. Bras. Cir. Cardiovasc., 2018, 33(2), 189-193.
[http://dx.doi.org/10.21470/1678-9741-2017-0201] [PMID: 29898150]
[4]
Zhao, Q.; Zhu, Y.; Xu, Z.; Cheng, Z.; Mei, J.; Chen, X.; Wang, X. Effect of ticagrelor plus aspirin, ticagrelor alone, or aspirin alone on saphenous vein graft patency 1 year after coronary artery bypass grafting: A randomized clinical trial. JAMA, 2018, 319(16), 1677-1686.
[http://dx.doi.org/10.1001/jama.2018.3197] [PMID: 29710164]
[5]
Zhang, K.; Cao, J.; Dong, R.; Du, J. Early growth response protein 1 promotes restenosis by upregulating intercellular adhesion molecule-1 in vein graft. Oxid. Med. Cell. Longev., 2013, 2013, 432409.
[http://dx.doi.org/10.1155/2013/432409] [PMID: 24386503]
[6]
Podemska-Jedrzejczak, Z.; Malinska, A.; Sujka-Kordowska, P.; Nowicki, M.; Puslecki, M.; Jemielity, M.; Perek, B. Vascular restenosis in coronary artery bypass grafting might be associated with VEGF-C/VEGFR-3 signaling pathway. Heart and Vessels, 2018, 33(9), 1106-1120.
[http://dx.doi.org/10.1007/s00380-018-1158-9] [PMID: 29557990]
[7]
Hassantash, S.A.; Bikdeli, B.; Kalantarian, S.; Sadeghian, M.; Afshar, H. Pathophysiology of aortocoronary saphenous vein bypass graft disease. Asian Cardiovasc. Thorac. Ann., 2008, 16(4), 331-336.
[http://dx.doi.org/10.1177/021849230801600418] [PMID: 18670032]
[8]
Muto, A.; Model, L.; Ziegler, K.; Eghbalieh, S.D.; Dardik, A. Mechanisms of vein graft adaptation to the arterial circulation: Insights into the neointimal algorithm and management strategies. Circ. J., 2010, 74(8), 1501-1512.
[http://dx.doi.org/10.1253/circj.CJ-10-0495] [PMID: 20606326]
[9]
Lu, Y.J.; Jan, Y.J.; Ko, B.S.; Liang, S.M.; Chen, L.; Wu, C.C.; Chin, C.H.; Kuo, C.C.; Yet, S.F.; Liou, J.Y. Expression of nik-related kinase in smooth muscle cells attenuates vascular inflammation and intimal hyperplasia. Aging, 2020, 12(8), 7511-7533.
[http://dx.doi.org/10.18632/aging.103104] [PMID: 32330120]
[10]
Tan, J.; Yang, L.; Liu, C.; Yan, Z. MicroRNA-26a targets MAPK6 to inhibit smooth muscle cell proliferation and vein graft neointimal hyperplasia. Sci. Rep., 2017, 7(1), 46602.
[http://dx.doi.org/10.1038/srep46602] [PMID: 28429763]
[11]
Bobi, J.; Garabito, M.; Solanes, N.; Cidad, P.; Ramos-Pérez, V.; Ponce, A.; Rigol, M.; Freixa, X.; Pérez-Martínez, C.; Pérez de Prado, A.; Fernández-Vázquez, F.; Sabaté, M.; Borrós, S.; López-López, J.R.; Pérez-García, M.T.; Roqué, M. Kv1.3 blockade inhibits proliferation of vascular smooth muscle cells in vitro and intimal hyperplasia in vivo. Transl. Res., 2020, 224, 40-54.
[http://dx.doi.org/10.1016/j.trsl.2020.06.002] [PMID: 32522668]
[12]
Liu, R.; Shen, H.; Ma, J.; Sun, L.; Wei, M. Extracellular vesicles derived from adipose mesenchymal stem cells regulate the phenotype of smooth muscle cells to limit intimal hyperplasia. Cardiovasc. Drugs Ther., 2016, 30(2), 111-118.
[http://dx.doi.org/10.1007/s10557-015-6630-5] [PMID: 26650931]
[13]
Cao, B.J.; Zhu, L.; Wang, X.W.; Zou, R.J.; Lu, Z.Q. MicroRNA-365 promotes the contractile phenotype of venous smooth muscle cells and inhibits neointimal formation in rat vein grafts. IUBMB Life, 2019, 71(7), 908-916.
[http://dx.doi.org/10.1002/iub.2022] [PMID: 30746857]
[14]
De Yébenes, V.G.; Briones, A.M.; Martos-Folgado, I.; Mur, S.M.; Oller, J.; Bilal, F.; González-Amor, M.; Méndez-Barbero, N.; Silla-Castro, J.C.; Were, F.; Jiménez-Borreguero, L.J.; Sánchez-Cabo, F.; Bueno, H.; Salaices, M.; Redondo, J.M.; Ramiro, A.R. Aging-associated miR-217 aggravates atherosclerosis and promotes cardiovascular dysfunction. Arterioscler. Thromb. Vasc. Biol., 2020, 40(10), 2408-2424.
[http://dx.doi.org/10.1161/ATVBAHA.120.314333] [PMID: 32847388]
[15]
Wang, H.W.; Huang, T.S.; Lo, H.H.; Huang, P.H.; Lin, C.C.; Chang, S.J.; Liao, K.H.; Tsai, C.H.; Chan, C.H.; Tsai, C.F.; Cheng, Y.C.; Chiu, Y.L.; Tsai, T.N.; Cheng, C.C.; Cheng, S.M. Deficiency of the microRNA-31-microRNA-720 pathway in the plasma and endothelial progenitor cells from patients with coronary artery disease. Arterioscler. Thromb. Vasc. Biol., 2014, 34(4), 857-869.
[http://dx.doi.org/10.1161/ATVBAHA.113.303001] [PMID: 24558106]
[16]
Amin, M.M.J.; Trevelyan, C.J.; Turner, N.A. MicroRNA-214 in health and disease. Cells, 2021, 10(12), 3274.
[http://dx.doi.org/10.3390/cells10123274] [PMID: 34943783]
[17]
Zhou, H.; Tang, W.; Yang, J.; Peng, J.; Guo, J.; Fan, C. MicroRNA-related strategies to improve cardiac function in heart failure. Front. Cardiovasc. Med., 2021, 8, 773083.
[http://dx.doi.org/10.3389/fcvm.2021.773083] [PMID: 34869689]
[18]
Anwar, M.A.; Saleh, A.I.; Al Olabi, R.; Al Shehabi, T.S.; Eid, A.H. Glucocorticoid-induced fetal origins of adult hypertension: Association with epigenetic events. Vascul. Pharmacol., 2016, 82, 41-50.
[http://dx.doi.org/10.1016/j.vph.2016.02.002] [PMID: 26903240]
[19]
Improta-Caria, A.C.; Aras, M.G.; Nascimento, L.; De Sousa, R.A.L.; Aras-Júnior, R.; Souza, B.S.F. MicroRNAs regulating renin-angiotensin-aldosterone system, sympathetic nervous system and left ventricular hypertrophy in systemic arterial hypertension. Biomolecules, 2021, 11(12), 1771.
[http://dx.doi.org/10.3390/biom11121771] [PMID: 34944415]
[20]
Park, J.H.; Kho, C. MicroRNAs and calcium signaling in heart disease. Int. J. Mol. Sci., 2021, 22(19), 10582.
[http://dx.doi.org/10.3390/ijms221910582] [PMID: 34638924]
[21]
Wehbe, N.; Nasser, S.A.; Pintus, G.; Badran, A.; Eid, A.H.; Baydoun, E. MicroRNAs in cardiac hypertrophy. Int. J. Mol. Sci., 2019, 20(19), E4714.
[http://dx.doi.org/10.3390/ijms20194714] [PMID: 31547607]
[22]
Dehaini, H.; Awada, H.; El-Yazbi, A.; Zouein, F.A.; Issa, K.; Eid, A.A.; Ibrahim, M.; Badran, A.; Baydoun, E.; Pintus, G.; Eid, A.H. MicroRNAs as potential pharmaco-targets in ischemia-reperfusion injury compounded by diabetes. Cells, 2019, 8(2), E152.
[http://dx.doi.org/10.3390/cells8020152] [PMID: 30759843]
[23]
Li, L.; Kang, L.; Zhao, W.; Feng, Y.; Liu, W.; Wang, T.; Mai, H.; Huang, J.; Chen, S.; Liang, Y.; Han, J.; Xu, X.; Ye, Q. miR-30a-5p suppresses breast tumor growth and metastasis through inhibition of LDHA-mediated warburg effect. Cancer Lett., 2017, 400, 89-98.
[http://dx.doi.org/10.1016/j.canlet.2017.04.034] [PMID: 28461244]
[24]
Maciejak, A.; Kostarska-Srokosz, E.; Gierlak, W.; Dluzniewski, M.; Kuch, M.; Marchel, M.; Opolski, G.; Kiliszek, M.; Matlak, K.; Dobrzycki, S.; Lukasik, A.; Segiet, A.; Sygitowicz, G.; Sitkiewicz, D.; Gora, M.; Burzynska, B. Circulating miR-30a-5p as a prognostic biomarker of left ventricular dysfunction after acute myocardial infarction. Sci. Rep., 2018, 8(1), 9883.
[http://dx.doi.org/10.1038/s41598-018-28118-1] [PMID: 29959359]
[25]
Pyo, J.O.; Yoo, S.M.; Ahn, H.H.; Nah, J.; Hong, S.H.; Kam, T.I.; Jung, S.; Jung, Y.K. Overexpression of ATG5 in mice activates autophagy and extends lifespan. Nat. Commun., 2013, 4(1), 2300.
[http://dx.doi.org/10.1038/ncomms3300] [PMID: 23939249]
[26]
Li, B.B.; Chen, Y.L.; Pang, F. MicroRNA-30a targets ATG5 and attenuates airway fibrosis in asthma by suppressing autophagy. Inflamm., 2020, 43(1), 44-53.
[http://dx.doi.org/10.1007/s10753-019-01076-0] [PMID: 31748850]
[27]
Yu, Y.; Yang, L.; Zhao, M.; Zhu, S.; Kang, R.; Vernon, P.; Tang, D.; Cao, L. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells. Leukemia, 2012, 26(8), 1752-1760.
[http://dx.doi.org/10.1038/leu.2012.65] [PMID: 22395361]
[28]
Qu, Q.; Bing, W.; Meng, X.; Xi, J.; Bai, X.; Liu, Q.; Guo, Y.; Zhao, X.; Bi, Y. Upregulation of miR-126-3p promotes human saphenous vein endothelial cell proliferation in vitro and prevents vein graft neointimal formation ex vivo and in vivo. Oncotarget, 2017, 8(63), 106790-106806.
[http://dx.doi.org/10.18632/oncotarget.22365] [PMID: 29290989]
[29]
West, N.E.; Qian, H.; Guzik, T.J.; Black, E.; Cai, S.; George, S.E.; Channon, K.M. Nitric Oxide Synthase (nNOS) gene transfer modifies venous bypass graft remodeling: Effects on vascular smooth muscle cell differentiation and superoxide production. Circulation, 2001, 104(13), 1526-1532.
[http://dx.doi.org/10.1161/hc3801.095693] [PMID: 11571247]
[30]
Ye, X.; Zhou, X.J.; Zhang, H. Exploring the role of Autophagy-Related Gene 5 (ATG5) yields important insights into autophagy in autoimmune/autoinflammatory diseases. Front. Immunol., 2018, 9, 2334.
[http://dx.doi.org/10.3389/fimmu.2018.02334] [PMID: 30386331]
[31]
Chen, M.Y.; Yadav, V.K.; Chu, Y.C.; Ong, J.R.; Huang, T.Y.; Lee, K.F.; Lee, K.H.; Yeh, C.T.; Lee, W.H. Hydroxychloroquine (HCQ) modulates autophagy and oxidative DNA damage stress in hepatocellular carcinoma to overcome sorafenib resistance via TLR9/SOD1/hsa-miR-30a-5p/Beclin-1 axis. Cancers, 2021, 13(13), 3227.
[http://dx.doi.org/10.3390/cancers13133227] [PMID: 34203465]
[32]
Hu, F.; Tao, X.; Zhao, L.; Guo, F.; Zhou, Q.; Song, H.; Xiang, H.; Shang, D. LncRNA-PVT1 aggravates severe acute pancreatitis by promoting autophagy via the miR-30a-5p/Beclin-1 axis. Am. J. Transl. Res., 2020, 12(9), 5551-5562.
[PMID: 33042437]
[33]
Yang, X.; Bai, F.; Xu, Y.; Chen, Y.; Chen, L. Intensified beclin-1 mediated by low expression of mir-30a-5p promotes chemoresistance in human small cell lung cancer. Cell. Physiol. Biochem., 2017, 43(3), 1126-1139.
[http://dx.doi.org/10.1159/000481754] [PMID: 28977798]
[34]
Gomez, D.; Owens, G.K. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc. Res., 2012, 95(2), 156-164.
[http://dx.doi.org/10.1093/cvr/cvs115] [PMID: 22406749]
[35]
Chen, P.Y.; Qin, L.; Li, G.; Tellides, G.; Simons, M. Fibroblast Growth Factor (FGF) signaling regulates Transforming Growth Factor Beta (TGFβ)-dependent smooth muscle cell phenotype modulation. Sci. Rep., 2016, 6(1), 33407.
[http://dx.doi.org/10.1038/srep33407] [PMID: 27634335]
[36]
Post, A.; Diaz-Rodriguez, P.; Balouch, B.; Paulsen, S.; Wu, S.; Miller, J.; Hahn, M.; Cosgriff-Hernandez, E. Elucidating the role of graft compliance mismatch on intimal hyperplasia using an ex vivo organ culture model. Acta Biomater., 2019, 89, 84-94.
[http://dx.doi.org/10.1016/j.actbio.2019.03.025] [PMID: 30878448]
[37]
Cheng, Y.; Liu, X.; Yang, J.; Lin, Y.; Xu, D.Z.; Lu, Q.; Deitch, E.A.; Huo, Y.; Delphin, E.S.; Zhang, C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ. Res., 2009, 105(2), 158-166.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.197517] [PMID: 19542014]
[38]
Wang, Y.; Dong, C.Q.; Peng, G.Y.; Huang, H.Y.; Yu, Y.S.; Ji, Z.C.; Shen, Z.Y. MicroRNA-134-5p regulates media degeneration through inhibiting VSMC phenotypic switch and migration in thoracic aortic dissection. Mol. Ther. Nucleic Acids, 2019, 16, 284-294.
[http://dx.doi.org/10.1016/j.omtn.2019.02.021] [PMID: 30951965]
[39]
Tan, H.; Yao, H.; Lie, Z.; Chen, G.; Lin, S.; Zhang, Y. MicroRNA‑30a‑5p promotes proliferation and inhibits apoptosis of human pulmonary artery endothelial cells under hypoxia by targeting YKL‑40. Mol. Med. Rep., 2019, 20(1), 236-244.
[http://dx.doi.org/10.3892/mmr.2019.10251] [PMID: 31115541]
[40]
Ormseth, M.J.; Solus, J.F.; Sheng, Q.; Chen, S.C.; Ye, F.; Wu, Q.; Oeser, A.M.; Allen, R.; Raggi, P.; Vickers, K.C.; Stein, C.M. Plasma miRNAs improve the prediction of coronary atherosclerosis in patients with rheumatoid arthritis. Clin. Rheumatol., 2021, 40(6), 2211-2219.
[http://dx.doi.org/10.1007/s10067-020-05573-8] [PMID: 33389220]
[41]
Ciavarella, C.; Motta, I.; Vasuri, F.; Fittipaldi, S.; Valente, S.; Pollutri, D.; Ricci, F.; Gargiulo, M.; Pasquinelli, G. Involvement of miR-30a-5p and miR-30d in endothelial to mesenchymal transition and early osteogenic commitment under inflammatory stress in HUVEC. Biomolecules, 2021, 11(2), 226.
[http://dx.doi.org/10.3390/biom11020226] [PMID: 33562690]
[42]
Liu, Y.F.; Spinelli, A.; Sun, L.Y.; Jiang, M.; Singer, D.V.; Ginnan, R.; Saddouk, F.Z.; Van Riper, D.; Singer, H.A. MicroRNA-30 inhibits neointimal hyperplasia by targeting Ca(2+)/Calmodulin-Dependent Protein Kinase IIδ (CaMKIIδ). Sci. Rep., 2016, 6(1), 26166.
[http://dx.doi.org/10.1038/srep26166] [PMID: 27199283]
[43]
Chu, P.; He, L.; Yang, C.; Zeng, W.; Huang, R.; Liao, L.; Li, Y.; Zhu, Z.; Wang, Y. Grass carp ATG5 and ATG12 promote autophagy but down-regulate the transcriptional expression levels of IFN-I signaling pathway. Fish Shellfish Immunol., 2019, 92, 600-611.
[http://dx.doi.org/10.1016/j.fsi.2019.06.014] [PMID: 31252046]
[44]
Huang, Q.; Liu, Y.; Zhang, S.; Yap, Y.T.; Li, W.; Zhang, D.; Gardner, A.; Zhang, L.; Song, S.; Hess, R.A.; Zhang, Z. Autophagy core protein ATG5 is required for elongating spermatid development, sperm individualization and normal fertility in male mice. Autophagy, 2020, 17(7), 1753-1767.
[PMID: 32677505]
[45]
Chen, D.; Tao, X.; Wang, Y.; Tian, F.; Wei, Y.; Chen, G.; Shen, H.; Wang, Z.; Yu, Z.; Li, H.; Chen, G. Curcumin accelerates reendothelialization and ameliorates intimal hyperplasia in balloon-injured rat carotid artery via the upregulation of endothelial cell autophagy. Int. J. Mol. Med., 2015, 36(6), 1563-1571.
[http://dx.doi.org/10.3892/ijmm.2015.2365] [PMID: 26459716]
[46]
Martinet, W.; De Meyer, G.R. Autophagy in atherosclerosis: A cell survival and death phenomenon with therapeutic potential. Circ. Res., 2009, 104(3), 304-317.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.188318] [PMID: 19213965]
[47]
Lin, X.; Li, S.; Zhao, Y.; Ma, X.; Zhang, K.; He, X.; Wang, Z. Interaction domains of p62: A bridge between p62 and selective autophagy. DNA Cell Biol., 2013, 32(5), 220-227.
[http://dx.doi.org/10.1089/dna.2012.1915] [PMID: 23530606]
[48]
Grootaert, M.O.J.; Moulis, M.; Roth, L.; Martinet, W.; Vindis, C.; Bennett, M.R.; De Meyer, G.R.Y. Vascular smooth muscle cell death, autophagy and senescence in atherosclerosis. Cardiovasc. Res., 2018, 114(4), 622-634.
[http://dx.doi.org/10.1093/cvr/cvy007] [PMID: 29360955]
[49]
Osonoi, Y.; Mita, T.; Azuma, K.; Nakajima, K.; Masuyama, A.; Goto, H.; Nishida, Y.; Miyatsuka, T.; Fujitani, Y.; Koike, M.; Mitsumata, M.; Watada, H. Defective autophagy in vascular smooth muscle cells enhances cell death and atherosclerosis. Autophagy, 2018, 14(11), 1991-2006.
[http://dx.doi.org/10.1080/15548627.2018.1501132] [PMID: 30025494]
[50]
Feng, X.; Zhang, H.; Meng, L.; Song, H.; Zhou, Q.; Qu, C.; Zhao, P.; Li, Q.; Zou, C.; Liu, X.; Zhang, Z. Hypoxia-induced acetylation of PAK1 enhances autophagy and promotes brain tumorigenesis via phosphorylating ATG5. Autophagy, 2020, 17(3), 723-742.
[PMID: 32186433]
[51]
He, R.; Yang, L.; Lin, X.; Chen, X.; Lin, X.; Wei, F.; Liang, X.; Luo, Y.; Wu, Y.; Gan, T.; Dang, Y.; Chen, G. MiR-30a-5p suppresses cell growth and enhances apoptosis of hepatocellular carcinoma cells via targeting AEG-1. Int. J. Clin. Exp. Pathol., 2015, 8(12), 15632-15641.
[PMID: 26884832]
[52]
Wang, L.; Zhao, S.; Yu, M. Mechanism of low expression of miR-30a-5p on epithelial-mesenchymal transition and metastasis in ovarian cancer. DNA Cell Biol., 2019, 38(4), 341-351.
[http://dx.doi.org/10.1089/dna.2018.4396] [PMID: 30839226]
[53]
Xiong, J.; Wei, B.; Ye, Q.; Liu, W. MiR-30a-5p/UBE3C axis regulates breast cancer cell proliferation and migration. Biochem. Biophys. Res. Commun., 2019, 516(3), 1013-1018.
[http://dx.doi.org/10.1016/j.bbrc.2016.03.069] [PMID: 27003255]
[54]
Cheng, C.C.; Yang, B.L.; Chen, W.C.; Ho, A.S.; Sie, Z.L.; Lin, H.C.; Chang, C.C. STAT3 mediated miR-30a-5p inhibition enhances proliferation and inhibits apoptosis in colorectal cancer cells. Int. J. Mol. Sci., 2020, 21(19), E7315.
[http://dx.doi.org/10.3390/ijms21197315] [PMID: 33023006]