Endocrine, Metabolic & Immune Disorders - Drug Targets

Author(s): Tanu Sharma, James A. Radosevich and Chandi C. Mandal*

DOI: 10.2174/1871530320666200519075908

Dual Role of microRNAs in Autophagy of Colorectal Cancer

Page: [56 - 66] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

Autophagy is an evolutionarily conserved pathway that eliminates unwanted proteins out of the cell and increases cell survival. However, dysfunctional autophagy is associated with cancer progression, cellular adaptation, cancer metastasis and makes it an attractive therapeutic target. MicroRNAs (miRNAs) are small single-stranded non-coding RNA molecules that usually bind to 3’UTR of mRNAs. This interaction eventually inhibits protein synthesis by repressing translation and/or by degrading mRNAs. miRNAs play a crucial role in the regulation of autophagy and also behave as both tumor suppressors and promoters in colorectal cancer. This paper defines an overall molecular view of how miRNAs regulate the dual role of autophagy in colorectal cancer. It also highlights how long noncoding RNAs modulate miRNAs expression to regulate autophagy in colorectal cancer. Thus, targeting autophagy by miRNAs seems to be a potential therapeutic strategy for colorectal cancer.

Keywords: Colorectal cancer, microRNA, autophagy, non-coding RNA, tumor suppressor, tumor promoter.

Graphical Abstract

[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Arnold, M.; Sierra, M.S.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global patterns and trends in colorectal cancer incidence and mortality. Gut, 2017, 66(4), 683-691.
[http://dx.doi.org/10.1136/gutjnl-2015-310912] [PMID: 26818619]
[3]
Zheng, Y.; Tan, K.; Huang, H. Long noncoding RNA HAGLROS regulates apoptosis and autophagy in colorectal cancer cells via sponging miR-100 to target ATG5 expression. J. Cell. Biochem., 2019, 120(3), 3922-3933.
[http://dx.doi.org/10.1002/jcb.27676] [PMID: 30430634]
[4]
D.A., Silva F.C.; Wernhoff, P.; Dominguez-Barrera, C.; Dominguez-Valentin, M. Update on hereditary colorectal cancer. Anticancer Res., 2016, 36(9), 4399-4405.
[http://dx.doi.org/10.21873/anticanres.10983] [PMID: 27630275]
[5]
Hahn, M.M.; de Voer, R.M.; Hoogerbrugge, N.; Ligtenberg, M.J.; Kuiper, R.P.; van Kessel, A.G. The genetic heterogeneity of colorectal cancer predisposition - guidelines for gene discovery. Cell Oncol. (Dordr.), 2016, 39(6), 491-510.
[http://dx.doi.org/10.1007/s13402-016-0284-6] [PMID: 27279102]
[6]
Jones, S.; Chen, W.D.; Parmigiani, G.; Diehl, F.; Beerenwinkel, N.; Antal, T.; Traulsen, A.; Nowak, M.A.; Siegel, C.; Velculescu, V.E.; Kinzler, K.W.; Vogelstein, B.; Willis, J.; Markowitz, S.D. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl. Acad. Sci. USA, 2008, 105(11), 4283-4288.
[http://dx.doi.org/10.1073/pnas.0712345105] [PMID: 18337506]
[7]
Binefa, G.; Rodríguez-Moranta, F.; Teule, A.; Medina-Hayas, M. Colorectal cancer: From prevention to personalized medicine. World J. Gastroenterol., 2014, 20(22), 6786-6808.
[http://dx.doi.org/10.3748/wjg.v20.i22.6786] [PMID: 24944469]
[8]
Sha, Q-K.; Chen, L.; Xi, J.Z.; Song, H. Long non-coding RNA LINC00858 promotes cells proliferation, migration and invasion by acting as a ceRNA of miR-22-3p in colorectal cancer. Artif. Cells Nanomed. Biotechnol., 2019, 47(1), 1057-1066.
[http://dx.doi.org/10.1080/21691401.2018.1544143] [PMID: 30931636]
[9]
Sridharan, M.; Hubbard, J.M.; Grothey, A. Colorectal cancer: How emerging molecular understanding affects treatment decisions. Oncology (Williston Park), 2014, 28(2), 110-118.
[PMID: 24701697]
[10]
Booton, R.; Lindsay, M.A. Emerging role of MicroRNAs and long noncoding RNAs in respiratory disease. Chest, 2014, 146(1), 193-204.
[http://dx.doi.org/10.1378/chest.13-2736] [PMID: 25010962]
[11]
Ding, L.; Lan, Z.; Xiong, X.; Ao, H.; Feng, Y.; Gu, H.; Yu, M.; Cui, Q. The dual role of microRNAs in colorectal cancer progression. Int. J. Mol. Sci., 2018, 19(9), 2791.
[http://dx.doi.org/10.3390/ijms19092791] [PMID: 30227605]
[12]
Jin, G.; Liu, Y.; Zhang, J.; Bian, Z.; Yao, S.; Fei, B.; Zhou, L.; Yin, Y.; Huang, Z. A panel of serum exosomal microRNAs as predictive markers for chemoresistance in advanced colorectal cancer. Cancer Chemother. Pharmacol., 2019, 84(2), 315-325.
[http://dx.doi.org/10.1007/s00280-019-03867-6] [PMID: 31089750]
[13]
Dikaiakos, P.; Gazouli, M.; Rizos, S.; Zografos, G.; Theodoropoulos, G.E. Evaluation of genetic variants in miRNAs in patients with colorectal cancer. Cancer Biomark., 2015, 15(2), 157-162.
[http://dx.doi.org/10.3233/CBM-140449] [PMID: 25519012]
[14]
Slattery, M.L.; Lee, F.Y.; Pellatt, A.J.; Mullany, L.E.; Stevens, J.R.; Samowitz, W.S.; Wolff, R.K.; Herrick, J.S. Infrequently expressed miRNAs in colorectal cancer tissue and tumor molecular phenotype. Mod. Pathol., 2017, 30(8), 1152-1169.
[http://dx.doi.org/10.1038/modpathol.2017.38] [PMID: 28548123]
[15]
Christensen, L.L.; Holm, A.; Rantala, J.; Kallioniemi, O.; Rasmussen, M.H.; Ostenfeld, M.S.; Dagnaes-Hansen, F.; Øster, B.; Schepeler, T.; Tobiasen, H.; Thorsen, K.; Sieber, O.M.; Gibbs, P.; Lamy, P.; Hansen, T.F.; Jakobsen, A.; Riising, E.M.; Helin, K.; Lubinski, J.; Hagemann-Madsen, R.; Laurberg, S.; Ørntoft, T.F.; Andersen, C.L. Functional screening identifies miRNAs influencing apoptosis and proliferation in colorectal cancer. PLoS One, 2014, 9(6)e96767
[http://dx.doi.org/10.1371/journal.pone.0096767] [PMID: 24892549]
[16]
Ashford, T.P.; Porter, K.R. Cytoplasmic components in hepatic cell lysosomes. J. Cell Biol., 1962, 12(1), 198-202.
[http://dx.doi.org/10.1083/jcb.12.1.198] [PMID: 13862833]
[17]
Choi, A.M.; Ryter, S.W.; Levine, B. Autophagy in human health and disease. N. Engl. J. Med., 2013, 368(7), 651-662.
[http://dx.doi.org/10.1056/NEJMra1205406] [PMID: 23406030]
[18]
Jardon, M.A. Autophagy: from structure to metabolism to therapeutic regulation; Taylor & Francis, 2013.
[19]
Ávalos, Y. Tumor suppression and promotion by autophagy. BioMed research international, 2014, 2014
[20]
Zhou, H.; Yuan, M.; Yu, Q.; Zhou, X.; Min, W.; Gao, D. Autophagy regulation and its role in gastric cancer and colorectal cancer. Cancer Biomark., 2016, 17(1), 1-10.
[http://dx.doi.org/10.3233/CBM-160613] [PMID: 27314289]
[21]
Humbert, M.; Medová, M.; Aebersold, D.M.; Blaukat, A.; Bladt, F.; Fey, M.F.; Zimmer, Y.; Tschan, M.P. Protective autophagy is involved in resistance towards MET inhibitors in human gastric adenocarcinoma cells. Biochem. Biophys. Res. Commun., 2013, 431(2), 264-269.
[http://dx.doi.org/10.1016/j.bbrc.2012.12.120] [PMID: 23313490]
[22]
Chaachouay, H.; Ohneseit, P.; Toulany, M.; Kehlbach, R.; Multhoff, G.; Rodemann, H.P. Autophagy contributes to resistance of tumor cells to ionizing radiation. Radiother. Oncol., 2011, 99(3), 287-292.
[http://dx.doi.org/10.1016/j.radonc.2011.06.002] [PMID: 21722986]
[23]
Wang, J.; Yang, K.; Zhou, L. Minhaowu.; Wu, Y.; Zhu, M.; Lai, X.; Chen, T.; Feng, L.; Li, M.; Huang, C.; Zhong, Q.; Huang, X. MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog., 2013, 9(10)e1003697
[http://dx.doi.org/10.1371/journal.ppat.1003697] [PMID: 24130493]
[24]
Frankel, L.B.; Wen, J.; Lees, M.; Høyer-Hansen, M.; Farkas, T.; Krogh, A.; Jäättelä, M.; Lund, A.H. microRNA-101 is a potent inhibitor of autophagy. EMBO J., 2011, 30(22), 4628-4641.
[http://dx.doi.org/10.1038/emboj.2011.331] [PMID: 21915098]
[25]
Pan, X.; Wang, Z.X.; Wang, R. MicroRNA-21: A novel therapeutic target in human cancer. Cancer Biol. Ther., 2010, 10(12), 1224-1232.
[http://dx.doi.org/10.4161/cbt.10.12.14252] [PMID: 21139417]
[26]
Javanmardi, S.; Aghamaali, M.R.; Abolmaali, S.S.; Mohammadi, S.; Tamaddon, A.M. miR-21, an oncogenic target miRNA for cancer therapy: molecular mechanisms and recent advancements in chemo and radio-resistance. Curr. Gene Ther., 2017, 16(6), 375-389.
[http://dx.doi.org/10.2174/1566523217666170102105119] [PMID: 28042781]
[27]
Hong, L.; Han, Y.; Zhang, Y.; Zhang, H.; Zhao, Q.; Wu, K.; Fan, D. MicroRNA-21: a therapeutic target for reversing drug resistance in cancer. Expert Opin. Ther. Targets, 2013, 17(9), 1073-1080.
[http://dx.doi.org/10.1517/14728222.2013.819853] [PMID: 23865553]
[28]
Chen, J-C.; Hsieh, Y.Y.; Lo, H.L.; Li, A.; Chou, C.J.; Yang, P.M. In vitro and in silico mechanistic insights into miR-21-5p-Mediated topoisomerase drug resistance in human colorectal cancer cells. Biomolecules, 2019, 9(9), 467.
[http://dx.doi.org/10.3390/biom9090467] [PMID: 31505885]
[29]
Liu, L.; Meng, T.; Wang, Q.S.; Jin, H.Z.; Sun, Z.Q.; Jin, B.; Fang, F.; Wang, H.J. Association of Beclin-1 and microRNA-30a expression with the severity and treatment response of colorectal cancer. Genet. Mol. Res., 2016, 15(2), 1-9.
[http://dx.doi.org/10.4238/gmr.15027704] [PMID: 27173217]
[30]
Su, M.; Wang, J.; Wang, C.; Wang, X.; Dong, W.; Qiu, W.; Wang, Y.; Zhao, X.; Zou, Y.; Song, L.; Zhang, L.; Hui, R. MicroRNA-221 inhibits autophagy and promotes heart failure by modulating the p27/CDK2/mTOR axis. Cell Death Differ., 2015, 22(6), 986-999.
[http://dx.doi.org/10.1038/cdd.2014.187] [PMID: 25394488]
[31]
Chen, Q.; Zhou, Y.; Richards, A.M.; Wang, P. Up-regulation of miRNA-221 inhibits hypoxia/reoxygenation-induced autophagy through the DDIT4/mTORC1 and Tp53inp1/p62 pathways. Biochem. Biophys. Res. Commun., 2016, 474(1), 168-174.
[http://dx.doi.org/10.1016/j.bbrc.2016.04.090] [PMID: 27105917]
[32]
Li, L.; Wang, Z.; Hu, X.; Wan, T.; Wu, H.; Jiang, W.; Hu, R. Human aortic smooth muscle cell-derived exosomal miR-221/222 inhibits autophagy via a PTEN/Akt signaling pathway in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun., 2016, 479(2), 343-350.
[http://dx.doi.org/10.1016/j.bbrc.2016.09.078] [PMID: 27644883]
[33]
Li, B.; Lu, Y.; Wang, H.; Han, X.; Mao, J.; Li, J.; Yu, L.; Wang, B.; Fan, S.; Yu, X.; Song, B. miR-221/222 enhance the tumorigenicity of human breast cancer stem cells via modulation of PTEN/Akt pathway. Biomed. Pharmacother., 2016, 79, 93-101.
[http://dx.doi.org/10.1016/j.biopha.2016.01.045] [PMID: 27044817]
[34]
Li, J.; Yao, L.; Li, G.; Ma, D.; Sun, C.; Gao, S.; Zhang, P.; Gao, F. miR-221 promotes epithelial-mesenchymal transition through targeting PTEN and forms a positive feedback loop with β-catenin/c-Jun signaling pathway in extra-hepatic cholangiocarcinoma. PLoS One, 2015, 10(10)e0141168
[http://dx.doi.org/10.1371/journal.pone.0141168] [PMID: 26501139]
[35]
Yang, W.; Yang, Y.; Xia, L.; Yang, Y.; Wang, F.; Song, M.; Chen, X.; Liu, J.; Song, Y.; Zhao, Y.; Yang, C. MiR-221 promotes capan-2 pancreatic ductal adenocarcinoma cells proliferation by targeting PTEN-Akt. Cell. Physiol. Biochem., 2016, 38(6), 2366-2374.
[http://dx.doi.org/10.1159/000445589] [PMID: 27230035]
[36]
Liao, D.; Li, T.; Ye, C.; Zeng, L.; Li, H.; Pu, X.; Ding, C.; He, Z.; Huang, G.L. miR-221 inhibits autophagy and targets TP53INP1 in colorectal cancer cells. Exp. Ther. Med., 2018, 15(2), 1712-1717.
[PMID: 29434757]
[37]
Xie, Y.; Zhao, J.; Liang, Y.; Chen, M.; Luo, Y.; Cui, X.; Jiang, B.; Peng, L.; Wang, X. MicroRNA-10b controls the metastasis and proliferation of colorectal cancer cells by regulating Krüppel-like factor 4. Artif. Cells Nanomed. Biotechnol., 2019, 47(1), 1722-1729.
[http://dx.doi.org/10.1080/21691401.2019.1606006] [PMID: 31032663]
[38]
Sun, C.; Wang, F.J.; Zhang, H.G.; Xu, X.Z.; Jia, R.C.; Yao, L.; Qiao, P.F. miR-34a mediates oxaliplatin resistance of colorectal cancer cells by inhibiting macroautophagy via transforming growth factor-β/Smad4 pathway. World J. Gastroenterol., 2017, 23(10), 1816-1827.
[http://dx.doi.org/10.3748/wjg.v23.i10.1816] [PMID: 28348487]
[39]
Hao, H.; Xia, G.; Wang, C.; Zhong, F.; Liu, L.; Zhang, D. miR-106a suppresses tumor cells death in colorectal cancer through targeting ATG7. Med. Mol. Morphol., 2017, 50(2), 76-85.
[http://dx.doi.org/10.1007/s00795-016-0150-7] [PMID: 27981410]
[40]
Sarver, A.L.; Li, L.; Subramanian, S. MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res., 2010, 70(23), 9570-9580.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2074] [PMID: 21118966]
[41]
Ueno, K.; Hirata, H.; Shahryari, V.; Deng, G.; Tanaka, Y.; Tabatabai, Z.L.; Hinoda, Y.; Dahiya, R. microRNA-183 is an oncogene targeting Dkk-3 and SMAD4 in prostate cancer. Br. J. Cancer, 2013, 108(8), 1659-1667.
[http://dx.doi.org/10.1038/bjc.2013.125] [PMID: 23538390]
[42]
Stiegelbauer, V.; Perakis, S.; Deutsch, A.; Ling, H.; Gerger, A.; Pichler, M. MicroRNAs as novel predictive biomarkers and therapeutic targets in colorectal cancer. World J. Gastroenterol., 2014, 20(33), 11727-11735.
[http://dx.doi.org/10.3748/wjg.v20.i33.11727] [PMID: 25206276]
[43]
Nugent, M.; Miller, N.; Kerin, M.J. MicroRNAs in colorectal cancer: function, dysregulation and potential as novel biomarkers. Eur. J. Surg. Oncol., 2011, 37(8), 649-654.
[http://dx.doi.org/10.1016/j.ejso.2011.05.005] [PMID: 21632200]
[44]
Wu, W.K.; Law, P.T.; Lee, C.W.; Cho, C.H.; Fan, D.; Wu, K.; Yu, J.; Sung, J.J. MicroRNA in colorectal cancer: From benchtop to bedside. Carcinogenesis, 2011, 32(3), 247-253.
[http://dx.doi.org/10.1093/carcin/bgq243] [PMID: 21081475]
[45]
Zhang, Q-H.; Sun, H.M.; Zheng, R.Z.; Li, Y.C.; Zhang, Q.; Cheng, P.; Tang, Z.H.; Huang, F. Meta-analysis of microRNA-183 family expression in human cancer studies comparing cancer tissues with noncancerous tissues. Gene, 2013, 527(1), 26-32.
[http://dx.doi.org/10.1016/j.gene.2013.06.006] [PMID: 23791657]
[46]
Huangfu, L.; Liang, H.; Wang, G.; Su, X.; Li, L.; Du, Z.; Hu, M.; Dong, Y.; Bai, X.; Liu, T.; Yang, B.; Shan, H. miR-183 regulates autophagy and apoptosis in colorectal cancer through targeting of UVRAG. Oncotarget, 2016, 7(4), 4735-4745.
[http://dx.doi.org/10.18632/oncotarget.6732] [PMID: 26717041]
[47]
Han, J.; Li, J.; Tang, K.; Zhang, H.; Guo, B.; Hou, N.; Huang, C. miR-338-3p confers 5-fluorouracil resistance in p53 mutant colon cancer cells by targeting the mammalian target of rapamycin. Exp. Cell Res., 2017, 360(2), 328-336.
[http://dx.doi.org/10.1016/j.yexcr.2017.09.023] [PMID: 28928082]
[48]
Yu, X.; Shi, W.; Zhang, Y.; Wang, X.; Sun, S.; Song, Z.; Liu, M.; Zeng, Q.; Cui, S.; Qu, X. CXCL12/CXCR4 axis induced miR-125b promotes invasion and confers 5-fluorouracil resistance through enhancing autophagy in colorectal cancer. Sci. Rep., 2017, 7, 42226.
[http://dx.doi.org/10.1038/srep42226] [PMID: 28176874]
[49]
Fujiya, M.; Konishi, H.; Mohamed Kamel, M.K.; Ueno, N.; Inaba, Y.; Moriichi, K.; Tanabe, H.; Ikuta, K.; Ohtake, T.; Kohgo, Y. microRNA-18a induces apoptosis in colon cancer cells via the autophagolysosomal degradation of oncogenic heterogeneous nuclear ribonucleoprotein A1. Oncogene, 2014, 33(40), 4847-4856.
[http://dx.doi.org/10.1038/onc.2013.429] [PMID: 24166503]
[50]
Chen, Z.; Gao, S.; Wang, D.; Song, D.; Feng, Y. Colorectal cancer cells are resistant to anti-EGFR monoclonal antibody through adapted autophagy. Am. J. Transl. Res., 2016, 8(2), 1190-1196.
[PMID: 27158405]
[51]
Taniguchi, K.; Sugito, N.; Kumazaki, M.; Shinohara, H.; Yamada, N.; Nakagawa, Y.; Ito, Y.; Otsuki, Y.; Uno, B.; Uchiyama, K.; Akao, Y. MicroRNA-124 inhibits cancer cell growth through PTB1/PKM1/PKM2 feedback cascade in colorectal cancer. Cancer Lett., 2015, 363(1), 17-27.
[http://dx.doi.org/10.1016/j.canlet.2015.03.026] [PMID: 25818238]
[52]
Hu, J.L.; He, G.Y.; Lan, X.L.; Zeng, Z.C.; Guan, J.; Ding, Y.; Qian, X.L.; Liao, W.T.; Ding, Y.Q.; Liang, L. Inhibition of ATG12-mediated autophagy by miR-214 enhances radiosensitivity in colorectal cancer. Oncogenesis, 2018, 7(2), 16.
[http://dx.doi.org/10.1038/s41389-018-0028-8] [PMID: 29459645]
[53]
Yang, X.; Xu, X.; Zhu, J.; Zhang, S.; Wu, Y.; Wu, Y.; Zhao, K.; Xing, C.; Cao, J.; Zhu, H.; Li, M.; Ye, Z.; Peng, W. miR-31 affects colorectal cancer cells by inhibiting autophagy in cancer-associated fibroblasts. Oncotarget, 2016, 7(48), 79617-79628.
[http://dx.doi.org/10.18632/oncotarget.12873] [PMID: 27793031]
[54]
Wang, Y.; Zhang, S.; Dang, S.; Fang, X.; Liu, M. Overexpression of microRNA-216a inhibits autophagy by targeting regulated MAP1S in colorectal cancer. OncoTargets Ther., 2019, 12, 4621-4629.
[http://dx.doi.org/10.2147/OTT.S196992] [PMID: 31354295]
[55]
Li, W.; Zou, J.; Yue, F.; Song, K.; Chen, Q.; McKeehan, W.L.; Wang, F.; Xu, G.; Huang, H.; Yi, J.; Liu, L. Defects in MAP1S-mediated autophagy cause reduction in mouse lifespans especially when fibronectin is overexpressed. Aging Cell, 2016, 15(2), 370-379.
[http://dx.doi.org/10.1111/acel.12441] [PMID: 26750654]
[56]
Zhai, H.; Song, B.; Xu, X.; Zhu, W.; Ju, J. Inhibition of autophagy and tumor growth in colon cancer by miR-502. Oncogene, 2013, 32(12), 1570-1579.
[http://dx.doi.org/10.1038/onc.2012.167] [PMID: 22580605]
[57]
Sümbül, A.T.; Göğebakan, B.; Ergün, S.; Yengil, E.; Batmacı, C.Y.; Tonyalı, Ö.; Yaldız, M. miR-204-5p expression in colorectal cancer: an autophagy-associated gene. Tumour Biol., 2014, 35(12), 12713-12719.
[http://dx.doi.org/10.1007/s13277-014-2596-3] [PMID: 25209181]
[58]
Ji, C.; Ju, S.; Qiang, J. miR-212 and mTOR form a regulation loop to modulate autophagy in colorectal adenoma HT-29 cells. Discov. Med., 2018, 25(140), 265-275.
[PMID: 30021100]
[59]
Tan, S.; Shi, H.; Ba, M.; Lin, S.; Tang, H.; Zeng, X.; Zhang, X. miR-409-3p sensitizes colon cancer cells to oxaliplatin by inhibiting Beclin-1-mediated autophagy. Int. J. Mol. Med., 2016, 37(4), 1030-1038.
[http://dx.doi.org/10.3892/ijmm.2016.2492] [PMID: 26935807]
[60]
Wei, R.; Yang, Q.; Han, B.; Li, Y.; Yao, K.; Yang, X.; Chen, Z.; Yang, S.; Zhou, J.; Li, M.; Yu, H.; Yu, M.; Cui, Q. microRNA-375 inhibits colorectal cancer cells proliferation by downregulating JAK2/STAT3 and MAP3K8/ERK signaling pathways. Oncotarget, 2017, 8(10), 16633-16641.
[http://dx.doi.org/10.18632/oncotarget.15114] [PMID: 28186962]
[61]
Zhang, R.; Xu, J.; Zhao, J.; Bai, J. Mir-30d suppresses cell proliferation of colon cancer cells by inhibiting cell autophagy and promoting cell apoptosis. Tumour Biol., 2017, 39(6)1010428317703984
[http://dx.doi.org/10.1177/1010428317703984] [PMID: 28651493]
[62]
Fu, Q.; Cheng, J.; Zhang, J.; Zhang, Y.; Chen, X.; Xie, J.; Luo, S. Downregulation of YEATS4 by miR-218 sensitizes colorectal cancer cells to L-OHP-induced cell apoptosis by inhibiting cytoprotective autophagy. Oncol. Rep., 2016, 36(6), 3682-3690.
[http://dx.doi.org/10.3892/or.2016.5195] [PMID: 27779719]
[63]
Zhai, H.; Fesler, A.; Ba, Y.; Wu, S.; Ju, J. Inhibition of colorectal cancer stem cell survival and invasive potential by hsa-miR-140-5p mediated suppression of Smad2 and autophagy. Oncotarget, 2015, 6(23), 19735-19746.
[http://dx.doi.org/10.18632/oncotarget.3771] [PMID: 25980495]
[64]
Liu, L.; Wang, H.J.; Meng, T.; Lei, C.; Yang, X.H.; Wang, Q.S.; Jin, B.; Zhu, J.F. lncRNA GAS5 Inhibits Cell Migration and Invasion and Promotes Autophagy by Targeting miR-222-3p via the GAS5/PTEN-Signaling Pathway in CRC. Mol. Ther. Nucleic Acids, 2019, 17, 644-656.
[http://dx.doi.org/10.1016/j.omtn.2019.06.009] [PMID: 31400607]
[65]
Liu, M.L.; Zhang, Q.; Yuan, X.; Jin, L.; Wang, L.L.; Fang, T.T.; Wang, W.B. Long noncoding RNA RP4 functions as a competing endogenous RNA through miR-7-5p sponge activity in colorectal cancer. World J. Gastroenterol., 2018, 24(9), 1004-1012.
[http://dx.doi.org/10.3748/wjg.v24.i9.1004] [PMID: 29531464]