Generic placeholder image

Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Mini-Review Article

miRNA as Regulators of Prostate Carcinogenesis and Endocrine and Chemoresistance

Author(s): Zoran Culig*

Volume 21, Issue 4, 2021

Published on: 07 January, 2021

Page: [283 - 288] Pages: 6

DOI: 10.2174/1568009620666210108103134

Price: $65

Abstract

More therapy options are available for advanced prostate cancer, including novel inhibitors of androgen synthesis, anti-androgens, chemotherapeutics and targeted therapies. Although patients ´ survival has been improved, management of castration therapy-resistant prostate cancer remains a challenge. Regulation of cellular events in cancer by small non-coding miRNAs is, therefore, an area of special interest. Overexpression of selected miRNA may lead to androgen independence and prostate cancer progression. miRNA may be considered also a biomarker in patients with prostate cancer. In contrast, diminished expression of tumor-suppressive miRNA in prostate cancer leads to enhanced proliferation, reduced apoptosis, increased migration, invasion and epithelial- to-mesenchymal transition. miRNA may be directly involved in the regulation of chemosensitivity in prostate cancer. Experimental overexpression of selected miRNA in chemoresistant prostate cancer leads to the inhibition of cellular stemness and epithelial-to-mesenchymal transition. Reduction of tumor-suppressive miRNA may also lead to hyperactivity of signaling pathways such as that of the epidermal growth factor receptor and mitogen-activated protein kinase. Although considerable progress on miRNA research in prostate cancer has been achieved, therapeutic effects could be improved on the basis of the development of novel delivery methods.

Keywords: Prostate cancer, miRNA, oncogenes, tumor suppressors, androgenic regulation, chemotherapy.

Graphical Abstract
[1]
Remmers, S.; Roobol, M.J. Personalized strategies in population screening for prostate cancer. Int. J. Cancer, 2020, 147(11), 2977-2987.
[http://dx.doi.org/10.1002/ijc.33045] [PMID: 32394421]
[2]
Uo, T.; Sprenger, C.C.; Plymate, S.R. Androgen receptor signaling and metabolic and cellular plasticity during progression to castration resistant prostate cancer. Front. Oncol., 2020, 10, 580617.
[http://dx.doi.org/10.3389/fonc.2020.580617] [PMID: 33163409]
[3]
Manceau, C.; Mourey, L.; Pouessel, D.; Ploussard, G. Abiraterone acetate in combination with prednisone in the treatment of prostate cancer: safety and efficacy. Expert Rev. Anticancer Ther., 2020, 20(8), 629-638.
[http://dx.doi.org/10.1080/14737140.2020.1785289] [PMID: 32552120]
[4]
Li, T.; Li, D.; Sha, J.; Sun, P.; Huang, Y. MicroRNA-21 directly targets MARCKS and promotes apoptosis resistance and invasion in prostate cancer cells. Biochem. Biophys. Res. Commun., 2009, 383(3), 280-285.
[http://dx.doi.org/10.1016/j.bbrc.2009.03.077] [PMID: 19302977]
[5]
Zhang, H.L.; Yang, L.F.; Zhu, Y.; Yao, X.D.; Zhang, S.L.; Dai, B.; Zhu, Y.P.; Shen, Y.J.; Shi, G.H.; Ye, D.W. Serum miRNA-21: elevated levels in patients with metastatic hormone-refractory prostate cancer and potential predictive factor for the efficacy of docetaxel-based chemotherapy. Prostate, 2011, 71(3), 326-331.
[http://dx.doi.org/10.1002/pros.21246] [PMID: 20842666]
[6]
Sun, T.; Wang, Q.; Balk, S.; Brown, M.; Lee, G.S.; Kantoff, P. The role of microRNA-221 and microRNA-222 in androgen-independent prostate cancer cell lines. Cancer Res., 2009, 69(8), 3356-3363.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-4112] [PMID: 19351832]
[7]
Sun, T.; Wang, X.; He, H.H.; Sweeney, C.J.; Liu, S.X.; Brown, M.; Balk, S.; Lee, G.S.; Kantoff, P.W. MiR-221 promotes the development of androgen independence in prostate cancer cells via downregulation of HECTD2 and RAB1A. Oncogene, 2014, 33(21), 2790-2800.
[http://dx.doi.org/10.1038/onc.2013.230] [PMID: 23770851]
[8]
Rane, J.K.; Scaravilli, M.; Ylipää, A.; Pellacani, D.; Mann, V.M.; Simms, M.S.; Nykter, M.; Collins, A.T.; Visakorpi, T.; Maitland, N.J. MicroRNA expression profile of primary prostate cancer stem cells as a source of biomarkers and therapeutic targets. Eur. Urol., 2015, 67(1), 7-10.
[http://dx.doi.org/10.1016/j.eururo.2014.09.005] [PMID: 25234358]
[9]
Cannistraci, A.; Federici, G.; Addario, A.; Di Pace, A.L.; Grassi, L.; Muto, G.; Collura, D.; Signore, M.; De Salvo, L.; Sentinelli, S.; Simone, G.; Costantini, M.; Nanni, S.; Farsetti, A.; Coppola, V.; De Maria, R.; Bonci, D. C-Met/miR-130b axis as novel mechanism and biomarker for castration resistance state acquisition. Oncogene, 2017, 36(26), 3718-3728.
[http://dx.doi.org/10.1038/onc.2016.505] [PMID: 28192399]
[10]
Wang, Y.; Lieberman, R.; Pan, J.; Zhang, Q.; Du, M.; Zhang, P.; Nevalainen, M.; Kohli, M.; Shenoy, N.K.; Meng, H.; You, M.; Wang, L. miR-375 induces docetaxel resistance in prostate cancer by targeting SEC23A and YAP1. Mol. Cancer, 2016, 15(1), 70.
[http://dx.doi.org/10.1186/s12943-016-0556-9] [PMID: 27832783]
[11]
Armstrong, C.M.; Liu, C.; Lou, W.; Lombard, A.P.; Evans, C.P.; Gao, A.C. MicroRNA-181a promotes docetaxel resistance in prostate cancer cells. Prostate, 2017, 77(9), 1020-1028.
[http://dx.doi.org/10.1002/pros.23358] [PMID: 28485104]
[12]
Guo, Y.; Cui, J.; Ji, Z.; Cheng, C.; Zhang, K.; Zhang, C.; Chu, M.; Zhao, Q.; Yu, Z.; Zhang, Y.; Fang, Y.X.; Gao, W.Q.; Zhu, H.H. miR-302/367/LATS2/YAP pathway is essential for prostate tumor-propagating cells and promotes the development of castration resistance. Oncogene, 2017, 36(45), 6336-6347.
[http://dx.doi.org/10.1038/onc.2017.240] [PMID: 28745315]
[13]
Hoey, C.; Ray, J.; Jeon, J.; Huang, X.; Taeb, S.; Ylanko, J.; Andrews, D.W.; Boutros, P.C.; Liu, S.K. miRNA-106a and prostate cancer radioresistance: a novel role for LITAF in ATM regulation. Mol. Oncol., 2018, 12(8), 1324-1341.
[http://dx.doi.org/10.1002/1878-0261.12328] [PMID: 29845714]
[14]
Fujita, Y.; Kojima, K.; Ohhashi, R.; Hamada, N.; Nozawa, Y.; Kitamoto, A.; Sato, A.; Kondo, S.; Kojima, T.; Deguchi, T.; Ito, M. MiR-148a attenuates paclitaxel resistance of hormone-refractory, drug-resistant prostate cancer PC3 cells by regulating MSK1 expression. J. Biol. Chem., 2010, 285(25), 19076-19084.
[http://dx.doi.org/10.1074/jbc.M109.079525] [PMID: 20406806]
[15]
Kojima, K.; Fujita, Y.; Nozawa, Y.; Deguchi, T.; Ito, M. MiR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate, 2010, 70(14), 1501-1512.
[http://dx.doi.org/10.1002/pros.21185] [PMID: 20687223]
[16]
Sikand, K.; Slaibi, J.E.; Singh, R.; Slane, S.D.; Shukla, G.C. miR 488* inhibits androgen receptor expression in prostate carcinoma cells. Int. J. Cancer, 2011, 129(4), 810-819.
[http://dx.doi.org/10.1002/ijc.25753] [PMID: 21710544]
[17]
Nadiminty, N.; Tummala, R.; Lou, W.; Zhu, Y.; Zhang, J.; Chen, X.; eVere White, R.W.; Kung, H.J.; Evans, C.P.; Gao, A.C. MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of Myc expression in prostate cancer cells. J. Biol. Chem., 2012, 287(2), 1527-1537.
[http://dx.doi.org/10.1074/jbc.M111.278705] [PMID: 22128178]
[18]
Albino, D.; Civenni, G.; Dallavalle, C.; Roos, M.; Jahns, H.; Curti, L.; Rossi, S.; Pinton, S.; D’Ambrosio, G.; Sessa, F.; Hall, J.; Catapano, C.V.; Carbone, G.M. Activation of the Lin28/let-7 axis by loss of ESE3/EHF promotes a tumorigenic and stem-like phenotype in prostate cancer. Cancer Res., 2016, 76(12), 3629-3643.
[http://dx.doi.org/10.1158/0008-5472.CAN-15-2665] [PMID: 27197175]
[19]
Fletcher, C.E.; Sulpice, E.; Combe, S.; Shibakawa, A.; Leach, D.A.; Hamilton, M.P.; Chrysostomou, S.L.; Sharp, A.; Welti, J.; Yuan, W.; Dart, D.A.; Knight, E.; Ning, J.; Francis, J.C.; Kounatidou, E.E.; Gaughan, L.; Swain, A.; Lupold, S.E.; de Bono, J.S.; McGuire, S.E.; Gidrol, X.; Bevan, C.L. Androgen receptor-modulatory microRNAs provide insight into therapy resistance and therapeutic targets in advanced prostate cancer. Oncogene, 2019, 38(28), 5700-5724.
[http://dx.doi.org/10.1038/s41388-019-0823-5] [PMID: 31043708]
[20]
Eedunuri, V.K.; Rajapakshe, K.; Fiskus, W.; Geng, C.; Chew, S.A.; Foley, C.; Shah, S.S.; Shou, J.; Mohamed, J.S.; Coarfa, C.; O’Malley, B.W.; Mitsiades, N. miR-137 targets p160 steroid receptor coctivators SRC1, SRC2, and SRC3 and inhibits cell proliferation. Mol. Endocrinol., 2015, 29(8), 1170-1183.
[http://dx.doi.org/10.1210/me.2015-1080] [PMID: 26066330]
[21]
Arora, V.K.; Schenkein, E.; Murali, R.; Subudhi, S.K.; Wongvipat, J.; Balbas, M.D.; Shah, N.; Cai, L.; Efstathiou, E.; Logothetis, C.; Zheng, D.; Sawyers, C.L. Glucocorticoid receptor confers resistance to antiandrogens by bypassing androgen receptor blockade. Cell, 2013, 155(6), 1309-1322.
[http://dx.doi.org/10.1016/j.cell.2013.11.012] [PMID: 24315100]
[22]
Puhr, M.; Hoefer, J.; Eigentler, A.; Ploner, C.; Handle, F.; Schaefer, G.; Kroon, J.; Leo, A.; Heidegger, I.; Eder, I.; Culig, Z.; Van der Pluijm, G.; Klocker, H. Glucocorticoid receptor is a key player for prostate cancer cell survival and a target for improved antiandrogen therapy. Clin. Cancer Res., 2018, 24(4), 927-938.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-0989] [PMID: 29158269]
[23]
Rane, J.K.; Erb, H.H.; Nappo, G.; Mann, V.M.; Simms, M.S.; Collins, A.T.; Visakorpi, T.; Maitland, N.J. Inhibition of the glucocorticoid receptor results in an enhanced miR-99a/100-mediated radiation response in stem-like cells from human prostate cancers. Oncotarget, 2016, 7(32), 51965-51980.
[http://dx.doi.org/10.18632/oncotarget.10207] [PMID: 27340920]
[24]
Xu, B.; Wang, N.; Wang, X.; Tong, N.; Shao, N.; Tao, J.; Li, P.; Niu, X.; Feng, N.; Zhang, L.; Hua, L.; Wang, Z.; Chen, M. MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate, 2012, 72(11), 1171-1178.
[http://dx.doi.org/10.1002/pros.22466] [PMID: 22161865]
[25]
Su, S.F.; Chang, Y.W.; Andreu-Vieyra, C.; Fang, J.Y.; Yang, Z.; Han, B.; Lee, A.S.; Liang, G. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene, 2013, 32(39), 4694-4701.
[http://dx.doi.org/10.1038/onc.2012.483] [PMID: 23085757]
[26]
Kao, C-J.; Martiniez, A.; Shi, X-B.; Yang, J.; Evans, C.P.; Dobi, A.; deVere White, R.W.; Kung, H.J. miR-30 as a tumor suppressor connects EGF/Src signal to ERG and EMT. Oncogene, 2014, 33(19), 2495-2503.
[http://dx.doi.org/10.1038/onc.2013.200] [PMID: 23728339]
[27]
Boll, K.; Reiche, K.; Kasack, K.; Mörbt, N.; Kretzschmar, A.K.; Tomm, J.M.; Verhaegh, G.; Schalken, J.; von Bergen, M.; Horn, F.; Hackermüller, J. MiR-130a, miR-203 and miR-205 jointly repress key oncogenic pathways and are downregulated in prostate carcinoma. Oncogene, 2013, 32(3), 277-285.
[http://dx.doi.org/10.1038/onc.2012.55] [PMID: 22391564]
[28]
Puhr, M.; Hoefer, J.; Schäfer, G.; Erb, H.H.; Oh, S.J.; Klocker, H.; Heidegger, I.; Neuwirt, H.; Culig, Z. Epithelial-to-mesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205. Am. J. Pathol., 2012, 181(6), 2188-2201.
[http://dx.doi.org/10.1016/j.ajpath.2012.08.011] [PMID: 23041061]
[29]
Fujita, Y.; Kojima, T.; Kawakami, K.; Mizutani, K.; Kato, T.; Deguchi, T.; Ito, M. miR-130a activates apoptotic signaling through activation of caspase-8 in taxane-resistant prostate cancer cells. Prostate, 2015, 75(14), 1568-1578.
[http://dx.doi.org/10.1002/pros.23031] [PMID: 26074357]
[30]
Sossey-Alaoui, K.; Plow, E.F. miR-138-mediated regulation of KINDLIN-2 expression modulates sensitivity to chemotherapeutics. Mol. Cancer Res., 2016, 14(2), 228-238.
[http://dx.doi.org/10.1158/1541-7786.MCR-15-0299] [PMID: 26474967]
[31]
Wen, D.; Peng, Y.; Lin, F.; Singh, R.K.; Mahato, R.I. Micellar delivery of miR-34a modulator rubone and paclitaxel in resistant prostate cancer. Cancer Res., 2017, 77(12), 3244-3254.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2355] [PMID: 28428276]
[32]
Du, H.; Wang, X.; Dong, R.; Hu, D.; Xiong, Y. miR-601 inhibits proliferation, migration and invasion of prostate cancer stem cells by targeting KRT5 to inactivate the Wnt signaling pathway. Int. J. Clin. Exp. Pathol., 2019, 12(12), 4361-4379.
[PMID: 31933840]
[33]
Che, Y.; Shi, X.; Shi, Y.; Jiang, X.; Ai, Q.; Shi, Y.; Gong, F.; Jiang, W. Exosomes derived from miR-143-overexpressing MSCs inhibit cell migration and invasion in human prostate cancer by downregulating TFF3. Mol. Ther. Nucleic Acids, 2019, 18, 232-244.
[http://dx.doi.org/10.1016/j.omtn.2019.08.010] [PMID: 31563120]
[34]
Guan, B.; Mu, L.; Zhang, L.; Wang, K.; Tian, J.; Xu, S.; Wang, X.; He, D.; Du, Y. MicroRNA-218 inhibits the migration, epithelial-mesenchymal transition and cancer stem cell properties of prostate cancer cells. Oncol. Lett., 2018, 16(2), 1821-1826.
[http://dx.doi.org/10.3892/ol.2018.8877] [PMID: 30008871]
[35]
Liu, T.; Chi, H.; Chen, J.; Chen, C.; Huang, Y.; Xi, H.; Xue, J.; Si, Y. Curcumin suppresses proliferation and in vitro invasion of human prostate cancer stem cells by ceRNA effect of miR-145 and lncRNA-ROR. Gene, 2017, 631, 29-38.
[http://dx.doi.org/10.1016/j.gene.2017.08.008] [PMID: 28843521]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy