Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Diagnostic Pathology
Published in: Diagnostic Pathology 1/2020

Open Access 01-12-2020 | Cytostatic Therapy | Review

Non coding RNAs as the critical factors in chemo resistance of bladder tumor cells

Authors: Amir Sadra Zangouei, Hamid Reza Rahimi, Majid Mojarrad, Meysam Moghbeli

Published in: Diagnostic Pathology | Issue 1/2020

Login to get access

Abstract

Background

Bladder cancer (BCa) is the ninth frequent and 13th leading cause of cancer related deaths in the world which is mainly observed among men. There is a declining mortality rates in developed countries. Although, the majority of BCa patients present Non-Muscle-Invasive Bladder Cancer (NMIBC) tumors, only 30% of patients suffer from muscle invasion and distant metastases. Radical cystoprostatectomy, radiation, and chemotherapy have proven to be efficient in metastatic tumors. However, tumor relapse is observed in a noticeable ratio of patients following the chemotherapeutic treatment. Non-coding RNAs (ncRNAs) are important factors during tumor progression and chemo resistance which can be used as diagnostic and prognostic biomarkers of BCa.

Main body

In present review we summarized all of the lncRNAs and miRNAs associated with chemotherapeutic resistance in bladder tumor cells.

Conclusions

This review paves the way of introducing a prognostic panel of ncRNAs for the BCa patients which can be useful to select a proper drug based on the lncRNA profiles of patients to reduce the cytotoxic effects of chemotherapy in such patients.
Literature
1.
Ploeg M, Aben KK, Kiemeney LA. The present and future burden of urinary bladder cancer in the world. World J Urol. 2009;27(3):289–93.
2.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.CrossRef
3.
Burger M, et al. Epidemiology and risk factors of urothelial bladder cancer. Eur Urol. 2013;63(2):234–41.CrossRef
4.
Amling CL. Diagnosis and management of superficial bladder cancer. Curr Probl Cancer. 2001;25(4):IN1-278.
5.
Sharma S, Ksheersagar P, Sharma P. Diagnosis and treatment of bladder cancer. Am Fam Physician. 2009;80(7):717–23.PubMed
6.
Stenzl A, et al. Treatment of muscle-invasive and metastatic bladder cancer: update of the EAU guidelines. Eur Urol. 2011;59(6):1009–18.CrossRef
7.
Martinez Rodriguez RH, Buisan Rueda O, Ibarz L. Bladder cancer: present and future. Med Clin (Barc). 2017;149(10):449–55.CrossRef
8.
Kim HL, Steinberg GD. The current status of bladder preservation in the treatment of muscle invasive bladder cancer. J Urol. 2000;164(3 Pt 1):627–32.CrossRef
9.
von der Maase H, Sengelov L, Roberts JT, Ricci S, Dogliotti L, Oliver T, Moore MJ, Zimmermann A, Arning M. Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J Clin Oncol. 2005;23(21):4602–8.
10.
Tanji N, et al. Long-term results of combined chemotherapy with gemcitabine and cisplatin for metastatic urothelial carcinomas. Int J Clin Oncol. 2010;15(4):369–75.CrossRef
11.
Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med. 2009;361(15):1475–85.CrossRef
12.
Lawrence MS, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013;499(7457):214–8.CrossRef
13.
Mojarrad M, Moghbeli M. Genetic and molecular biology of bladder cancer among Iranian patients. Mol Genet Genomic Med. 2020;8:e1233.CrossRef
14.
Ding B, et al. Non-coding RNA in drug resistance of hepatocellular carcinoma. Biosci Rep. 2018;38(5):BSR20180915.CrossRef
15.
Ma J, Dong C, Ji C. MicroRNA and drug resistance. Cancer Gene Ther. 2010;17(8):523–31.CrossRef
16.
Rahmani Z, Mojarrad M, Moghbeli M. Long non-coding RNAs as the critical factors during tumor progressions among Iranian population: an overview. Cell Biosci. 2020;10:6.CrossRef
17.
Chen J, Li Y, Li Z, Cao L. LncRNA MST1P2/miR-133b axis affects the chemoresistance of bladder cancer to cisplatin-based therapy via Sirt1/p53 signaling. J Biochem Mol Toxicol. 2020;34(4):e22452.
18.
Chen X, Liu M, Meng F, Sun B, Jin X, Jia C. The long noncoding RNA HIF1A-AS2 facilitates cisplatin resistance in bladder cancer. J Cell Biochem. 2019;120(1):243–52.
19.
Wu J, Li W, Ning J, Yu W, Rao T, Cheng F. Long noncoding RNA UCA1 targets miR-582-5p and contributes to the progression and drug resistance of bladder cancer cells through ATG7-mediated autophagy inhibition. Onco Targets Ther. 2019;12:495.
20.
Zhang H, Guo Y, Song Y, Shang C. Long noncoding RNA GAS5 inhibits malignant proliferation and chemotherapy resistance to doxorubicin in bladder transitional cell carcinoma. Cancer Chemother Pharmacol. 2017;79(1):49–55.
21.
Liu P, Li X, Cui Y, Chen J, Li C, Li Q, Li H, Zhang X, Zu X. LncRNA-MALAT1 mediates cisplatin resistance via miR-101-3p/VEGF-C pathway in bladder cancer. Acta Biochim Biophys Sin. 2019;51(11):1148–57.
22.
Li B, Xie D, Zhang H. Long non-coding RNA GHET1 contributes to chemotherapeutic resistance to Gemcitabine in bladder cancer. Cancer Chemother Pharmacol. 2019;84(1):187–94.
23.
An Q, Zhou L, Xu N. Long noncoding RNA FOXD2-AS1 accelerates the gemcitabine-resistance of bladder cancer by sponging miR-143. Biomed Pharmacother. 2018;103:415–20.
24.
Wang H, Li Q, Niu X, Wang G, Zheng S, Fu G, Wang Z. miR-143 inhibits bladder cancer cell proliferation and enhances their sensitivity to gemcitabine by repressing IGF-1R signaling. Oncol Lett. 2017;13(1):435–40.
25.
Fan Y, Shen B, Tan M, Mu X, Qin Y, Zhang F, Liu Y. Long non-coding RNA UCA 1 increases chemoresistance of bladder cancer cells by regulating Wnt signaling. FEBS J. 2014;281(7):1750–8.
26.
Pan J, Li XU, Wu W, Xue M, Hou H, Zhai W, Chen W. Long non-coding RNA UCA1 promotes cisplatin/gemcitabine resistance through CREB modulating miR-196a-5p in bladder cancer cells. Cancer Lett. 2016;382(1):64–76.
27.
Xie D, Zhang H, Hu X, Shang C. Knockdown of long non-coding RNA Taurine Up-Regulated 1 inhibited doxorubicin resistance of bladder urothelial carcinoma via Wnt/β-catenin pathway. Oncotarget. 2017;8(51):88689.
28.
Xie D, Zhang H, Shang C. Long non-coding RNA CDKN2B antisense RNA 1 gene inhibits Gemcitabine sensitivity in bladder urothelial carcinoma. J Cancer. 2018;9(12):2160.
29.
Zhuang J, Shen L, Yang L, Huang X, Lu Q, Cui Y, Zheng X, Zhao X, Zhang D, Huang R, Guo H. TGFβ1 promotes gemcitabine resistance through regulating the LncRNA-LET/NF90/miR-145 signaling axis in bladder cancer. Theranostics. 2017;7(12):3053.
30.
Li Y, Shi B, Dong F, Zhu X, Liu B, Liu Y. Long non-coding RNA DLEU1 promotes cell proliferation, invasion and confers cisplatin resistance in bladder cancer by regulating the miR-99b/HS3ST3B1 axis. Front Genet. 2019;10:280.
31.
Zhao W, Li W, Jin X, Niu T, Cao Y, Zhou P, Zheng M. Silencing long non-coding RNA NEAT1 enhances the suppression of cell growth, invasion, and apoptosis of bladder cancer cells under cisplatin chemotherapy. Int J Clin Exp Pathol. 2019;12(2):549.
32.
Xiao J, Niu S, Zhu J, Lv L, Deng H, Pan D, Shen D, Xu C, Shen Z, Tao T. miR-22-3p enhances multi-chemoresistance by targeting NET1 in bladder cancer cells. Oncol Rep. 2018;39(6):2731–40.
33.
Deng Y, Bai H, Hu H. rs11671784 G/A variation in miR-27a decreases chemo-sensitivity of bladder cancer by decreasing miR-27a and increasing the target RUNX-1 expression. Biochem Biophys Res Commun. 2015;458(2):321–7.
34.
Drayton RM, Dudziec E, Peter S, Bertz S, Hartmann A, Bryant HE, Catto JW. Reduced expression of miRNA-27a modulates cisplatin resistance in bladder cancer by targeting the cystine/glutamate exchanger SLC7A11. Clin Cancer Res. 2014;20(7):1990–2000.
35.
Bu Q, Fang Y, Cao Y, Chen Q, Liu Y. Enforced expression of miR-101 enhances cisplatin sensitivity in human bladder cancer cells by modulating the cyclooxygenase-2 pathway. Mol Med Rep. 2014;10(4):2203–9.
36.
Vinall RL, Ripoll AZ, Wang S, Pan CX, deVere White RW. MiR-34a chemosensitizes bladder cancer cells to cisplatin treatment regardless of p53-Rb pathway status. Int J Cancer. 2012;130(11):2526–38.
37.
Li H, Yu G, Shi R, Lang B, Chen X, Xia D, Xiao H, Guo X, Guan W, Ye Z, Xiao W. Cisplatin-induced epigenetic activation of miR-34a sensitizes bladder cancer cells to chemotherapy. Mol Cancer. 2014;13(1):1-1.
38.
Liu X, Liu X, Wu Y, Fang Z, Wu Q, Wu C, Hao Y, Yang X, Zhao J, Li J, Wang Q. MicroRNA-34a attenuates metastasis and chemoresistance of bladder cancer cells by targeting the TCF1/LEF1 axis. Cell Physiol Biochem. 2018;48(1):87–98.
39.
Zhang Q, Zhuang J, Deng Y, Yang L, Cao W, Chen W, Lin T, Lv X, Yu H, Xue Y, Guo H. miR34a/GOLPH3 axis abrogates urothelial bladder cancer chemoresistance via reduced cancer stemness. Theranostics. 2017;7(19):4777.
40.
Tan Y, Zhang T, Zhou L, Liu S, Liang C. MiR-34b-3p represses the multidrug-chemoresistance of bladder cancer cells by regulating the CCND2 and P2RY1 genes. Med Sci Monit. 2019;25:1323.
41.
Luan T, Fu S, Huang L, Zuo Y, Ding M, Li N, Chen J, Wang H, Wang J. MicroRNA-98 promotes drug resistance and regulates mitochondrial dynamics by targeting LASS2 in bladder cancer cells. Exp Cell Res. 2018;373(1–2):188–97.
42.
Li B, Xie D, Zhang H. MicroRNA-101-3p advances cisplatin sensitivity in bladder urothelial carcinoma through targeted silencing EZH2. J Cancer. 2019;10(12):2628.
43.
Cao J, Wang Q, Wu G, Li S, Wang Q. miR-129-5p inhibits gemcitabine resistance and promotes cell apoptosis of bladder cancer cells by targeting Wnt5a. Int Urol Nephrol. 2018;50(10):1811–9.
44.
Lv L, Li Y, Deng H, Zhang C, Pu Y, Qian L, Xiao J, Zhao W, Liu Q, Zhang D, Wang Y. MiR-193a-3p promotes the multi-chemoresistance of bladder cancer by targeting the HOXC9 gene. Cancer Lett. 2015;357(1):105–13.
45.
Deng H, Lv L, Li Y, Zhang C, Meng F, Pu Y, Xiao J, Qian L, Zhao W, Liu Q, Zhang D. The miR-193a-3p regulated PSEN1 gene suppresses the multi-chemoresistance of bladder cancer. Biochimica et Biophysica Acta (BBA)- Mol Basis Dis. 2015;1852(3):520–8.
46.
Lin SR, Yeh HC, Wang WJ, Ke HL, Lin HH, Hsu WC, Chao SY, Hour TC, Wu WJ, Pu YS, Huang AM. MiR-193b mediates CEBPD-induced cisplatin sensitization through targeting ETS1 and cyclin D1 in human urothelial carcinoma cells. J Cell Biochem. 2017;118(6):1563–73.
47.
Deng H, Lv L, Li Y, Zhang C, Meng F, Pu Y, Xiao J, Qian L, Zhao W, Liu Q, Zhang D. miR-193a-3p regulates the multi-drug resistance of bladder cancer by targeting the LOXL4 gene and the oxidative stress pathway. Mol Cancer. 2014;13(1):234.
48.
Lv L, Deng H, Li Y, Zhang C, Liu X, Liu Q, Zhang D, Wang L, Pu Y, Zhang H, He Y. The DNA methylation-regulated miR-193a-3p dictates the multi-chemoresistance of bladder cancer via repression of SRSF2/PLAU/HIC2 expression. Cell Death Dis. 2014;5(9):e1402–2.
49.
Shindo T, Niinuma T, Nishiyama N, Shinkai N, Kitajima H, Kai M, Maruyama R, Tokino T, Masumori N, Suzuki H. Epigenetic silencing of miR-200b is associated with cisplatin resistance in bladder cancer. Oncotarget. 2018;9(36):24457.
50.
Zhang X, Zhang Y, Liu X, Fang A, Li P, Li Z, Liu T, Yang Y, Du L, Wang C. MicroRNA-203 is a prognostic indicator in bladder cancer and enhances chemosensitivity to cisplatin via apoptosis by targeting Bcl-w and survivin. PloS One. 2015;10(11):e0143441.
51.
Liu J, Bi J, Li Z, Li Z, Liu X, Kong C. miR-214 reduces cisplatin resistance by targeting netrin-1 in bladder cancer cells. Int J Mol Med. 2018;41(3):1765–73.
52.
Li P, Yang X, Cheng Y, Zhang X, Yang C, Deng X, Li P, Tao J, Yang H, Wei J, Tang J. MicroRNA-218 increases the sensitivity of bladder cancer to cisplatin by targeting Glut1. Cell Physiol Biochem. 2017;41(3):921–32.
53.
Zeng LP, Hu ZM, Li K, Xia K. miR-222 attenuates cisplatin-induced cell death by targeting the PPP 2R2A/Akt/mTOR Axis in bladder cancer cells. J Cell Mol Med. 2016;20(3):559–67.
54.
Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012;40(14):6391–400.
55.
Anastasiadou E, Jacob LS, Slack FJJNRC. Non-coding RNA networks in cancer. Nat Rev Cancer. 2018;18(1):5.
56.
Dong P, Xiong Y, Yue J, Hanley SJ, Kobayashi N, Todo Y, Watari H. Long non-coding RNA NEAT1: a novel target for diagnosis and therapy in human tumors. Front Genet. 2018;9:471.
57.
Malek E, Jagannathan S, Driscoll JJJO. Correlation of long non-coding RNA expression with metastasis, drug resistance and clinical outcome in cancer. Oncotarget. 2014;5(18):8027.
58.
Massari F, Santoni M, Ciccarese C, Brunelli M, Conti A, Santini D, Montironi R, Cascinu S, Tortora G. Emerging concepts on drug resistance in bladder cancer: Implications for future strategies. Crit Rev Oncol Hematol. 2015;96(1):81–90.
59.
Yafi FA, North S, Kassouf W. First-and second-line therapy for metastatic urothelial carcinoma of the bladder. Curr Oncol. 2011;18(1):e25.
60.
Revollo JR, Grimm AA, Imai SI. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J Biol Chem. 2004;279(49):50754–63.
61.
Zhang Y, Huang W, Ran Y, Xiong Y, Zhong Z, Fan X, Wang Z, Ye Q. miR-582-5p inhibits proliferation of hepatocellular carcinoma by targeting CDK1 and AKT3. Tumor Biol. 2015;36(11):8309–16.
62.
Zhang X, Zhang Y, Yang J, Li S, Chen J. Upregulation of miR-582-5p inhibits cell proliferation, cell cycle progression and invasion by targeting Rab27a in human colorectal carcinoma. Cancer Gene Ther. 2015;22(10):475–80.
63.
Wang WW, Chen B, Lei CB, Liu GX, Wang YG, Yi C, Wang YY, Zhang SY. miR-582-5p inhibits invasion and migration of salivary adenoid cystic carcinoma cells by targeting FOXC1. Jpn J Clin Oncol. 2017;47(8):690–8.
64.
Geng J, Klionsky DJ. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. EMBO reports. 2008;9(9):859–64.
65.
Jia L, Yang A. Noncoding RNAs in therapeutic resistance of cancer. Adv Exp Med Biol. 2016;927:265–95.CrossRef
66.
Fang Z, Chen W, Yuan Z, Liu X, Jiang H. LncRNA-MALAT1 contributes to the cisplatin-resistance of lung cancer by upregulating MRP1 and MDR1 via STAT3 activation. Biomed Pharmacother. 2018;101:536–42.
67.
Zhang X, Bo P, Liu L, Zhang X, Li J. Overexpression of long non-coding RNA GHET1 promotes the development of multidrug resistance in gastric cancer cells. Biomed Pharmacother. 2017;92:580–5.
68.
Niedersuess-Beke D, Puntus T, Kunit T, Gruenberger B, Lamche M, Loidl W, Böhm R, Kraischits N, Kudlacek S, Schramek P, Meran JG. Neoadjuvant chemotherapy with gemcitabine plus cisplatin in patients with locally advanced bladder cancer. Oncology. 2017;93(1):36–42.
69.
Ostwal V, Pinninti R, Ramaswamy A, Shetty N, Goel M, Patkar S, Mirani J, Nashikkar C, Banavali S. Treatment of advanced Gall bladder cancer in the real world—can continuation chemotherapy improve outcomes?. J Gastrointest Oncol. 2017;8(2):368.
70.
Su F, He W, Chen C, Liu M, Liu H, Xue F, Bi J, Xu D, Zhao Y, Huang J, Lin T. The long non-coding RNA FOXD2-AS1 promotes bladder cancer progression and recurrence through a positive feedback loop with Akt and E2F1. Cell Death Dis. 2018;9(2):1–17.
71.
Rubin R, Baserga R. Insulin-like growth factor I receptor. Its role in cell proliferation, apoptosis and tumorigenicity. Lab Invest. 1995;73(3):311–31.
72.
Hanahan D, Weinberg RA. The hallmarks of cancer. cell. 2000;100(1):57–70.
73.
Baserga RJTib. Controlling IGF-receptor function: a possible strategy for tumor therapy. Trends Biotechnol. 1996;14(5):150–2.
74.
Qian X, Yu J, Yin Y, He J, Wang L, Li Q, Zhang LQ, Li CY, Shi ZM, Xu Q, Li W. MicroRNA-143 inhibits tumor growth and angiogenesis and sensitizes chemosensitivity to oxaliplatin in colorectal cancers. Cell Cycle. 2013;12(9):1385–94.
75.
Zheng HC. The molecular mechanisms of chemoresistance in cancers. Oncotarget. 2017;8(35):59950–64.CrossRef
76.
Wang F, et al. UCA1, a non-protein-coding RNA up-regulated in bladder carcinoma and embryo, influencing cell growth and promoting invasion. FEBS Lett. 2008;582(13):1919–27.
77.
Abbaszadegan MR, et al. WNT and NOTCH signaling pathways as activators for epidermal growth factor receptor in esophageal squamous cell carcinoma. Cell Mol Biol Lett. 2018;23:42.CrossRef
78.
Moghbeli M, et al. Correlation of Wnt and NOTCH pathways in esophageal squamous cell carcinoma. J Cell Commun Signal. 2016;10(2):129–35.CrossRef
79.
Wang F, Zhou J, Xie X, Hu J, Chen L, Hu Q, Guo H, Yu C. Involvement of SRPK1 in cisplatin resistance related to long non-coding RNA UCA1 in human ovarian cancer cells. Neoplasm. 2015;62(3):432–8.
80.
Cheng N, et al. Long non-coding RNA UCA1 induces non-T790M acquired resistance to EGFR-TKIs by activating the AKT/mTOR pathway in EGFR-mutant non-small cell lung cancer. Oncotarget. 2015;6(27):23582.
81.
Ren K, Li Z, Li Y, Zhang W, Han X. Long noncoding RNA taurine-upregulated gene 1 promotes cell proliferation and invasion in gastric cancer via negatively modulating miRNA-145-5p. Oncol Res Featuring Preclinical Clin Cancer Ther. 2017;25(5):789–98.
82.
Zhai HY, Sui MH, Yu X, Qu Z, Hu JC, Sun HQ, Zheng HT, Zhou K, Jiang LX. Overexpression of long non-coding RNA TUG1 promotes colon cancer progression. Med Sci Monit. 2016;22:3281.
83.
Wang L, et al. Long non-coding RNA TUG1 promotes colorectal cancer metastasis via EMT pathway. Oncotarget. 2016;7(32):51713.
84.
Qin CF, Zhao FL. Long non-coding RNA TUG1 can promote proliferation and migration of pancreatic cancer via EMT pathway. Eur Rev Med Pharmacol Sci.2017;21(10):2377–84.
85.
Iliev R, Kleinova R, Juracek J, Dolezel J, Ozanova Z, Fedorko M, Pacik D, Svoboda M, Stanik M, Slaby O. Overexpression of long non-coding RNA TUG1 predicts poor prognosis and promotes cancer cell proliferation and migration in high-grade muscle-invasive bladder cancer. Tumor Biol. 2016;37(10):13385–90.
86.
Liu J, et al. Prognostic role of lncRNA TUG1 for cancer outcome: evidence from 840 cancer patients. Oncotarget. 2017;8(30):50051.
87.
Hanušová V, Boušová I, Skálová L. Possibilities to increase the effectiveness of doxorubicin in cancer cells killing. Drug Metab Rev. 2011;43(4):540–57.
88.
Huang MD, Chen WM, Qi FZ, Xia R, Sun M, Xu TP, Yin L, Zhang EB, De W, Shu YQ. Long non-coding RNA ANRIL is upregulated in hepatocellular carcinoma and regulates cell proliferation by epigenetic silencing of KLF2. J Hematol Oncol. 2015;8(1):57–7.
89.
Zou ZW, Ma C, Medoro L, Chen L, Wang B, Gupta R, Liu T, Yang XZ, Chen TT, Wang RZ, Zhang WJ. LncRNA ANRIL is up-regulated in nasopharyngeal carcinoma and promotes the cancer progression via increasing proliferation, reprograming cell glucose metabolism and inducing side-population stem-like cancer cells. Oncotarget. 2016;7(38):61741.
90.
Liu B, et al. Expression and mechanisms of long non-coding RNA genes MEG3 and ANRIL in gallbladder cancer. Tumor Biol. 2016;37(7):9875–86.
91.
de Sousa Cavalcante L, Monteiro G. Gemcitabine: metabolism and molecular mechanisms of action, sensitivity and chemoresistance in pancreatic cancer. Eur J Pharmacol. 2014;741:8–16.
92.
Roussos ET, et al. AACR special conference on epithelial-mesenchymal transition and cancer progression and treatment. AACR. 2010.
93.
Vumbaca F, et al. Double-stranded RNA-binding protein regulates vascular endothelial growth factor mRNA stability, translation, and breast cancer angiogenesis. Mol Cell Biol. 2008;28(2):772–83.
94.
Shim J, et al. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol Cell. 2002;10(6):1331–44.
95.
Kuwano Y, et al. NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res. 2010;38(1):225–38.
96.
Yang F, et al. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cancer. 2013;49(6):1083–96.
97.
Liu T, et al. LncRNA DLEU1 contributes to colorectal cancer progression via activation of KPNA3. Mol Cancer. 2018;17(1):118.
98.
Zhang S, et al. Long non-coding RNA DLEU1 exerts an oncogenic function in non-small cell lung cancer. Biomed Pharmacother. 2019;109:985–90.
99.
Wang LL, et al. DLEU 1 contributes to ovarian carcinoma tumourigenesis and development by interacting with miR-490-3p and altering CDK 1 expression. J Cell Mol Med. 2017;21(11):3055–65.
100.
Gao S, et al. Long noncoding RNA DLEU1 aggravates pancreatic ductal adenocarcinoma carcinogenesis via the miR-381/CXCR4 axis. J Cell Physiol. 2019;234(5):6746–57.
101.
Parasramka M, et al. BAP1 dependent expression of long non-coding RNA NEAT-1 contributes to sensitivity to gemcitabine in cholangiocarcinoma. Mol Cancer. 2017;16(1):1–22.
102.
Jiang P, et al. NEAT1 upregulates EGCG-induced CTR1 to enhance cisplatin sensitivity in lung cancer cells. Oncotarget. 2016;7(28):43337.
103.
Ru Y, et al. neaT1_2–sFPQ axis mediates cisplatin resistance in liver cancer cells in vitro. Onco Taget Ther. 2018;11:5695.
104.
Hu Y, et al. Knockdown of the oncogene lncRNA NEAT1 restores the availability of miR-34c and improves the sensitivity to cisplatin in osteosarcoma. Biosci Rep. 2018;38(3).
105.
Nordentoft I, et al. miRNAs associated with chemo-sensitivity in cell lines and in advanced bladder cancer. BMC Med Genomics. 2012;5(1):40.
106.
Duan R, Pak C, Jin P. Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum Mol Genet. 2007;16(9):1124–31.
107.
Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol. 2009;27(34):5848.
108.
Diestra JE, et al. Expression of multidrug resistance proteins P-glycoprotein, multidrug resistance protein 1, breast cancer resistance protein and lung resistance related protein in locally advanced bladder cancer treated with neoadjuvant chemotherapy: biological and clinical implications. J Urol. 2003;170(4):1383–7.
109.
Pastore A, et al. Analysis of glutathione: implication in redox and detoxification. Clinica chimica acta. 2003;333(1):19–39.
110.
Russo A, et al. Selective modulation of glutathione levels in human normal versus tumor cells and subsequent differential response to chemotherapy drugs. Cancer Res. 1986;46(6):2845–8.
111.
Wu G, et al. Glutathione metabolism and its implications for health. J Nutr. 2004;134(3):489–92.
112.
Sato H, et al. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem. 1999;274(17):11455–8.
113.
Greenhough A, et al. The COX-2/PGE 2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinog. 2009;30(3):377–86.
114.
Hasegawa K, et al. Overcoming paclitaxel resistance in uterine endometrial cancer using a COX-2 inhibitor. Oncol Rep. 2013;30(6):2937–44.
115.
He XP, et al. Downregulation of miR-101 in gastric cancer correlates with cyclooxygenase-2 overexpression and tumor growth. FEBS J. 2012;279(22):4201–12.
116.
Lodygin D, et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle. 2008;7(16):2591–600.
117.
Wiggins JF, et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010;70(14):5923–30.
118.
Ji X, Wang Z, Geamanu A, Goja A, Sarkar FH, Gupta SV. Delta-tocotrienol suppresses Notch-1 pathway by upregulating miR-34a in nonsmall cell lung cancer cells. Int J Cancer. 2012;131(11):2668–77.
119.
Nakatani F, et al. miR-34a predicts survival of Ewing's sarcoma patients and directly influences cell chemo-sensitivity and malignancy. J Pathol. 2012;226(5):796–805.
120.
Li Y, et al. Amplification of LAPTM4B and YWHAZ contributes to chemotherapy resistance and recurrence of breast cancer. Nat Med. 2010;16(2):214.
121.
He L, et al. A microRNA component of the p53 tumour suppressor network. Nature. 2007;447(7148):1130–4.
122.
Tarasov V, et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell cycle. 2007;6(13):1586–93.
123.
Chang T-C, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell. 2007;26(5):745–52.
124.
Yang YM, Chang JW. Bladder cancer initiating cells (BCICs) are among EMA− CD44v6+ subset: novel methods for isolating undetermined cancer stem (initiating) cells. Cancer Invest. 2008;26(7):725–33.
125.
Kuncova J, et al. Expression of CD44v6 correlates with cell proliferation and cellular atypia in urothelial carcinoma cell lines 5637 and HT1197. Folia Biol (Praha). 2005;51(1):3–11.
126.
Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J, Chang HY, van de Rijn M, Shortliffe L. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci. 2009;106(33):14016–21.
127.
Scott KL, Kabbarah O, Liang MC, Ivanova E, Anagnostou V, Wu J, Dhakal S, Wu M, Chen S, Feinberg T, Huang J. GOLPH3 modulates mTOR signalling and rapamycin sensitivity in cancer. Nature. 2009;459(7250):1085–90.
128.
Zhang Q, et al. GOLPH3 is a potential therapeutic target and a prognostic indicatior of poor survival in bladder cancer treated by cystectomy. Oncotarget. 2015;6(31):32177.
129.
Raghavan D. Molecular targeting and pharmacogenomics in the management of advanced bladder cancer. Interdiscip Intern J Am Cancer Soc. 2003;97(S8):2083–9.
130.
Shariat SF, et al. p53 expression in patients with advanced urothelial cancer of the urinary bladder. BJU Int. 2010;105(4):489–95.
131.
Shariat SF, et al. p53 predictive value for pT1–2 N0 disease at radical cystectomy. J Urol. 2009;182(3):907–13.
132.
Castillo-Martin M, et al. Molecular pathways of urothelial development and bladder tumorigenesis. In: Urologic oncology: seminars and original investigations. Amsterdam: Elsevier; 2010.
133.
Kim JE, Lou Z, Chen J. Interactions between DBC1 and SIRT1 are deregulated in breast cancer cells. Cell Cycle. 2009;8(22):3784–5.
134.
Rodon J, Perez J, Kurzrock R. Combining targeted therapies: practical issues to consider at the bench and bedside. Oncologist. 2010;15(1):37.
135.
Zhang F, et al. MicroRNA-2682-3p inhibits osteosarcoma cell proliferation by targeting CCND2, MMP8 and Myd88. Oncol Lett. 2018;16(3):3359–64.
136.
Hu W, et al. MiR-373-3p enhances the chemosensitivity of gemcitabine through cell cycle pathway by targeting CCND2 in pancreatic carcinoma cells. Biomed Pharmacother. 2018;105:887–98.
137.
Volonté C, D’Ambrosi N. Membrane compartments and purinergic signalling: the purinome, a complex interplay among ligands, degrading enzymes, receptors and transporters. FEBS J. 2009;276(2):318–29.
138.
Smyth SS, et al. G-protein–coupled receptors as signaling targets for antiplatelet therapy. Arterioscler Thromb Vasc Biol. 2009;29(4):449–57.
139.
Gremmel T, et al. Synergistic inhibition of both P2Y1 and P2Y12 adenosine diphosphate receptors as novel approach to rapidly attenuate platelet-mediated thrombosis. Arterioscler Thromb Vasc Biol. 2016;36(3):501–9.
140.
Yanachkov IB, et al. New highly active antiplatelet agents with dual specificity for platelet P2Y1 and P2Y12 adenosine diphosphate receptors. Eur J Med Chem. 2016;107:204–18.
141.
Li X-N, et al. Circular RNA circVAPA is up-regulated and exerts oncogenic properties by sponging miR-101 in colorectal cancer. Biomed Pharmacother. 2019;112:108611.
142.
Li C-Y, et al. Clinical value of miR-101-3p and biological analysis of its prospective targets in breast cancer: a study based on The Cancer Genome Atlas (TCGA) and bioinformatics. Med Sci Monit. 2017;23:1857.
143.
Jin Q, et al. MicroRNA-101-3p inhibits proliferation in retinoblastoma cells by targeting EZH2 and HDAC9. Exp Ther Med. 2018;16(3):1663–70.
144.
Liu D, et al. LncRNA SPRY4-IT1 sponges miR-101-3p to promote proliferation and metastasis of bladder cancer cells through up-regulating EZH2. Cancer Lett. 2017;388:281–91.
145.
Yamagishi M, Uchimaru K. Targeting EZH2 in cancer therapy. Curr Opin Oncol. 2017;29(5):375–81.
146.
Lu JF, Pokharel D, Bebawy M. Bebawy, MRP1 and its role in anticancer drug resistance. Drug Metab Rev. 2015;47(4):406–19.
147.
Zhang Y-K, et al. Multidrug resistance proteins (MRPs) and cancer therapy. AAPS J. 2015;17(4):802–12.
148.
Yan X, et al. Visfatin mediates doxorubicin resistance in human colorectal cancer cells via up regulation of multidrug resistance 1 (MDR1). Cancer Chemother Pharmacol. 2017;80(2):395–403.
149.
Anghel R, et al. Outcome of urinary bladder cancer after combined therapies. J Med Life. 2016;9(2):153.
150.
Moghbeli M, et al. Role of Msi1 and MAML1 in regulation of Notch signaling pathway in patients with esophageal squamous cell carcinoma. J Gastrointest Cancer. 2015;46(4):365–9.
151.
Moghbeli M, et al. Role of MAML1 in targeted therapy against the esophageal cancer stem cells. J Transl Med. 2019;17(1):126.
152.
Ma Z, et al. MiR-129-5p inhibits non-small cell lung cancer cell stemness and chemoresistance through targeting DLK1. Biochem Biophys Res Commun. 2017;490(2):309–16.
153.
Oishi I, et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells. 2003;8(7):645–54.
154.
Ishitani T, et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca2+ pathway to antagonize Wnt/β-catenin signaling. Mol Cell Biol. 2003;23(1):131–9.
155.
Topol L, et al. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3–independent β-catenin degradation. J Cell Biol. 2003;162(5):899–908.
156.
Hung T-H, et al. Wnt5A regulates ABCB1 expression in multidrug-resistant cancer cells through activation of the non-canonical PKA/β-catenin pathway. Oncotarget. 2014;5(23):12273.
157.
Asem MS, et al. Wnt5a signaling in cancer. Cancers. 2016;8(9):79.
158.
Wolff EM, Liang G, Jones PAJNcpU. Mechanisms of disease: genetic and epigenetic alterations that drive bladder cancer. Nat Clin Pract Urol. 2005;2(10):502–10.
159.
Chen H, et al. Evaluation of diagnostic accuracy of DNA methylation biomarkers for bladder cancer: a systematic review and meta-analysis. Biomarkers. 2014;19(3):189–97.
160.
Kandimalla R, Van Tilborg AA, Zwarthoff ECJNRU. DNA methylation-based biomarkers in bladder cancer. Nat Rev Urol. 2013;10(6):327.
161.
Anglim PP, et al. Identification of a panel of sensitive and specific DNA methylation markers for squamous cell lung cancer. Mol Cancer. 2008;7(1):62.
162.
Nakano H, et al. Gain-of-function microRNA screens identify miR-193a regulating proliferation and apoptosis in epithelial ovarian cancer cells. Int J Oncol. 2013;42(6):1875–82.
163.
Li Y, et al. Epigenetic silencing of microRNA-193a contributes to leukemogenesis in t (8; 21) acute myeloid leukemia by activating the PTEN/PI3K signal pathway. Blood, J Am Soc Hematol. 2013;121(3):499–509.
164.
Brunkan AL, Goate AM. Presenilin function and γ-secretase activity. J Neurochemistry. 2005;93(4):769–92.
165.
Cho S, Lu M, He X, Ee PL, Bhat U, Schneider E, Miele L, Beck WT. Notch1 regulates the expression of the multidrug resistance gene ABCC1/MRP1 in cultured cancer cells. Proc Natl Acad Sci. 2011;108(51):20778–83.
166.
Balamurugan K, Sterneck E. The many faces of C/EBPδ and their relevance for inflammation and cancer. Int J Biol Sci. 2013;9(9):917.
167.
Ko CY, Chang WC, Wang JM. Biological roles of CCAAT/Enhancer-binding protein delta during inflammation. J Biomed Sci. 2015;22(1):6.
168.
Pulido-Salgado M, Vidal-Taboada JM, Saura J. C/EBPβ and C/EBPδ transcription factors: basic biology and roles in the CNS. Prog Neurobiol. 2015;132:1–33.
169.
Iliopoulos D, Rotem A, Struhl K. Inhibition of miR-193a expression by Max and RXRα activates K-Ras and PLAU to mediate distinct aspects of cellular transformation. Cancer Res. 2011;71(15):5144–53.
170.
Gao X, et al. MicroRNA-193a represses c-kit expression and functions as a methylation-silenced tumor suppressor in acute myeloid leukemia. Oncogene. 2011;30(31):3416–28.
171.
Han J-W, et al. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat Genet. 2009;41(11):1234.
172.
Bittel D, et al. Refining the 22q11. 2 deletion breakpoints in DiGeorge syndrome by aCGH. Cytogenet Genome Res. 2009;124(2):113–20.
173.
Cazalla D, et al. Nuclear export and retention signals in the RS domain of SR proteins. Mol Cell Biol. 2002;22(19):6871–82.
174.
Young TM, et al. The human I-mfa domain-containing protein, HIC, interacts with cyclin T1 and modulates P-TEFb-dependent transcription. Mol Cell Biol. 2003;23(18):6373–84.
175.
Kanazawa S, et al. c-Myc recruits P-TEFb for transcription, cellular proliferation and apoptosis. Oncogene. 2003;22(36):5707–11.
176.
Gregory PA, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593–601.
177.
Park S-M, et al. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008;22(7):894–907.
178.
De Caceres II, et al. IGFBP-3 hypermethylation-derived deficiency mediates cisplatin resistance in non-small-cell lung cancer. Oncogene. 2010;29(11):1681–90.
179.
von Karstedt S, Montinaro A, Walczak HJNRC. Exploring the TRAILs less travelled: TRAIL in cancer biology and therapy. Nat Rev Cancer. 2017;17(6):352.
180.
Herr HW, et al. Defining optimal therapy for muscle invasive bladder cancer. J Urol. 2007;177(2):437–43.
181.
Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001;15(22):2922–33.
182.
Dohi T, et al. An IAP-IAP complex inhibits apoptosis. J Biol Chem. 2004;279(33):34087–90.
183.
Zhang J, et al. miR-214 promotes apoptosis and sensitizes breast cancer cells to doxorubicin by targeting the RFWD2-p53 cascade. Biochem Biophys Res Commun. 2016;478(1):337–42.
184.
Yu X, et al. MiR-214 increases the sensitivity of breast cancer cells to tamoxifen and fulvestrant through inhibition of autophagy. Mol Cancer. 2015;14(1):208.
185.
Li Q-Q, et al. Sulforaphane inhibits cancer stem-like cell properties and cisplatin resistance through miR-214-mediated downregulation of c-MYC in non-small cell lung cancer. Oncotarget. 2017;8(7):12067.
186.
Han G, et al. microRNA-218 inhibits prostate cancer cell growth and promotes apoptosis by repressing TPD52 expression. Biochem Biophys Res Commun. 2015;456(3):804–9.
187.
Wang J, et al. MicroRNA-214 suppresses oncogenesis and exerts impact on prognosis by targeting PDRG1 in bladder cancer. PloS One. 2015;10(2).
188.
Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–78.
189.
Galluzzi L, et al. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31(15):1869–83.
190.
Moreno-Sánchez R, et al. Energy metabolism in tumor cells. FEBS J. 2007;274(6):1393–418.
191.
Wong QW, Ching AK, Chan AW, Choy KW, To KF, Lai PB, Wong N. MiR-222 overexpression confers cell migratory advantages in hepatocellular carcinoma through enhancing AKT signaling. Clin Cancer Res. 2010;16(3):867–75.
192.
Gan R, Yang Y, Yang X, Zhao L, Lu J, Meng QH. Downregulation of miR-221/222 enhances sensitivity of breast cancer cells to tamoxifen through upregulation of TIMP 3. Cancer Gene Ther. 2014;21(7):290–6.
193.
Yang YF, Wang F, Xiao JJ, Song Y, Zhao YY, Cao Y, Bei YH, Yang CQ. MiR-222 overexpression promotes proliferation of human hepatocellular carcinoma HepG2 cells by downregulating p27. Int J Clin experimental Med. 2014;7(4):893.
194.
Garofalo M, Quintavalle C, Romano G, M croce C, Condorelli G. miR221/222 in cancer: their role in tumor progression and response to therapy. Curr Mol Med. 2012;12(1):27–33.
195.
SSchönthal AH. Role of serine/threonine protein phosphatase 2A in cancer. Cancer Lett. 2001;170(1):1–13.
196.
Virshup DM. Protein phosphatase 2A: a panoply of enzymes. Curr Opin Cell Biol. 2000;12(2):180–5.
197.
Janssens V, Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J. 2001;353(3):417–39.
Metadata
Title
Non coding RNAs as the critical factors in chemo resistance of bladder tumor cells
Authors
Amir Sadra Zangouei
Hamid Reza Rahimi
Majid Mojarrad
Meysam Moghbeli
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Diagnostic Pathology / Issue 1/2020
Electronic ISSN: 1746-1596
DOI
https://doi.org/10.1186/s13000-020-01054-3

Other articles of this Issue 1/2020

Diagnostic Pathology 1/2020 Go to the issue

Research

Clinicopathologic features of infection-related glomerulonephritis with IgA deposits: a French Nationwide study

Research

Role of hypoxia-related proteins in adenoid cystic carcinoma invasion

Case Report

Parathyroid carcinoma with sarcomatoid differentiation: a case report and literature review

Research

Expression of FAM83H and ZNF16 are associated with shorter survival of patients with gallbladder carcinoma

Case Report

Ovarian mesonephric-like adenocarcinoma arising in serous borderline tumor: a case report with complex morphological and molecular analysis

Research

Semantic segmentation to identify bladder layers from H&E Images