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

Volumn 6, Issue 27, 2015, Pages 23582-23593

  Cheng, Ningning ^a   Cai, Weijing ^a   Ren, Shengxiang ^a   Li, Xuefei ^a   Wang, Qi ^a   Pan, Hui ^a   Zhao, Mingchuan ^a   Li, Jiayu ^a   Zhang, Yishi ^a   Zhao, Chao ^a   Chen, Xiaoxia ^a   Fei, Ke ^a   Zhou, Caicun ^a   Hirsch, Fred R ^b  

^a TONGJI UNIVERSITY   (China)

^b UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

Acquired resistance; EGFR TKIs; Non small cell lung cancer; UCA1

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; LONG UNTRANSLATED RNA; MAMMALIAN TARGET OF RAPAMYCIN; NERVE CELL ADHESION MOLECULE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; VIMENTIN; ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR; SMALL INTERFERING RNA; TARGET OF RAPAMYCIN KINASE; UCA1 RNA, HUMAN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PROGNOSIS; CANCER RESISTANCE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROGRESSION FREE SURVIVAL; SIGNAL TRANSDUCTION; UCA1 GENE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DISEASE FREE SURVIVAL; DRUG RESISTANCE; GENETICS; IMMUNOHISTOCHEMISTRY; LUNG TUMOR; METABOLISM; MULTIVARIATE ANALYSIS; MUTATION; NUDE MOUSE; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; MICE; MICE, NUDE; MULTIVARIATE ANALYSIS; MUTATION; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, LONG NONCODING; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES; TREATMENT OUTCOME; UP-REGULATION;

EID: 84943421796     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4361     Document Type: Article

References (45)

1. Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhou SW, Ren SX, Lu S, Zhang L, Hu CP, et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802):a multicentre, open-label, randomised, phase 3 study. Lancet Oncol. 2011;12:735-742.
2. Keedy VL, Temin S, Somerfield MR, Beasley MB, Johnson DH, McShane LM, Milton DT, Strawn JR, Wakelee HA, Giaccone G. American Society of Clinical Oncology provisional clinical opinion:epidermal growth factor receptor (EGFR) mutation testing for patients with advanced non-small-cell lung cancer considering firstline EGFR tyrosine kinase inhibitor therapy. J Clin Oncol. 2011;29:2121-2127.
3. Han SW, Kim TY, Hwang PG, Jeong S, Kim J, Choi IS, Oh DY, Kim YT, Kim DW, Chung DH, Im SA, Kim YT, Lee JS, et al. Predictive and prognostic impact of epidermal growth factor receptor mutation in non-smallcell lung cancer patients treated with gefitinib. J Clin Oncol. 2005;23:2493-2501.
4. Somaiah N, Fidler MJ, Garrett-Mayer E, Wahlquist A, Shirai K, Buckingham L, Hensing T, Bonomi P, Simon GR. Epidermal growth factor receptor (EGFR) mutations are exceptionally rare in thyroid transcription factor (TTF-1)-negative adenocarcinomas of the lung. Oncoscience. 2014;1:522-528.
5. Gainor JF, Shaw AT. Emerging paradigms in the development of resistance to tyrosine kinase inhibitors in lung cancer. J Clin Oncol. 2013;31:3987-3996.
6. Wang Y, Xia H, Zhuang Z, Miao L, Chen X, Cai H. Axlaltered microRNAs regulate tumorigenicity and gefitinib resistance in lung cancer. Cell Death Dis. 2014;5:e1227.
7. Arcila ME, Oxnard GR, Nafa K, Riely GJ, Solomon SB, Zakowski MF, Kris MG, Pao W, Miller VA, Ladanyi M. Rebiopsy of lung cancer patients with acquired resistance to EGFR inhibitors and enhanced detection of the T790M mutation using a locked nucleic acid-based assay. Clin Cancer Res. 2011;17:1169-1180.
8. Bar J, Onn A. Overcoming molecular mechanisms of resistance to first-generation epidermal growth factor receptor tyrosine kinase inhibitors. Clin Lung Cancer. 2012;13:267-279.
9. Hammerman PS, Jänne PA, Johnson BE. Resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res. 2009;15:7502-7509.
10. Ohashi K, Maruvka YE, Michor F, Pao W. Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J Clin Oncol. 2013;31:1070-1080.
11. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet. 2011;12:861-874.
12. Cheetham SW, Gruhl F, Mattick JS, Dinger ME. Long noncoding RNAs and the genetics of cancer. Br J Cancer. 2013;108:2419-2425.
13. Tsang WP, Kwok TT. Riboregulator H19 induction of MDR1-associated drug resistance in human hepatocellular carcinoma cells. Oncogene. 2007;26:4877-4881.
14. Tsang WP, Wong TW, Cheung AH, Co CN, Kwok TT. Induction of drug resistance and transformation in human cancer cells by the noncoding RNA CUDR. RNA. 2007;13:890-898.
15. Yang Y, Li H, Hou S, Hu B, Liu J, Wang J. The noncoding RNA expression profile and the effect of lncRNA AK126698 on cisplatin resistance in non-small-cell lung cancer cell. PLoS One. 2013;8:e65309.
16. Cheng NN, Li CF, Zhao C, Ren SX, Chen XX, Cai WJ, Zhao MC, Zhang YS, Li JY, Wang Q, Zhou CC. Microarray expression profile of long non-coding RNAs in EGFR-TKIs resistance of human non-small cell lung cancer. Oncology Rep. 2015;33:833-839.
17. Cappuzzo F, Magrini E, Ceresoli GL, Bartolini S, Rossi E, Ludovini V, Gregorc, V, Ligorio, C, Cancellieri, A, Damiani, S, Spreafico, A, Paties, C. T, Lombardo, L, et al. Akt phosphorylation and gefitinib efficacy in patients with advanced non-small-cell lung cancer. J Natl Cancer Inst. 2004;96:1133-1141.
18. Xie M, He CS, Wei SH, Zhang L. Notch-1 contributes to epidermal growth factor receptor tyrosine kinase inhibitor acquired resistance in non-small cell lung cancer in vitro and in vivo. Eur J Cancer. 2013;49:3559-3572.
19. Tam WL, Weinberg RA. The epigenetics of epithelialmesenchymal plasticity in cancer. Nat Med. 2013;19:1438-1449.
20. Bird A. Perceptions of epigenetics. Nature. 2007;447:396-398.
21. Costa FF. Non-coding RNAs, epigenetics and complexity. Gene. 2008;410:9-17.
22. Li B, Ren S, Li X, Wang Y, Garfield D, Zhou S, Chen, X, Su, C, Chen, M, Kuang, P, Gao, G, He, Y, Fan, L, et al. MiR-21 overexpression is associated with acquired resistance of EGFR-TKI in non-small cell lung cancer. Lung Cancer. 2014;83:146-153.
23. Wang YS, Wang YH, Xia HP, Zhou SW, Schmid-Bindert G, Zhou CC. MicroRNA-214 regulates the acquired resistance to gefitinib via the PTEN/AKT pathway in EGFR-mutant cell lines. Asian Pac J Cancer Prev. 2012;13:255-260.
24. Wang Y, Chen W, Yang C, Wu W, Wu S, Qin X, Li X. Long non-coding RNA UCA1a(CUDR) promotes proliferation and tumorigenesis of bladder cancer. Int J Oncol. 2012;41:276-284.
25. Wang F, Li X, Xie X, Zhao L, Chen W. UCA1, a nonprotein-coding RNA up-regulated in bladder carcinoma and embryo, influencing cell growth and promoting invasion. FEBS Lett. 2008;582:1919-1927.
26. Fan Y, Shen B, Tan M, Mu X, Qin Y, Zhang F, Liu Y. Long non-coding RNA UCA1 increases chemoresistances of bladder cancer cells by regulating Wnt signaling. FEBS J. 2014;281:1750-1758.
27. Li H, Schmid-Bindert G, Wang D, Zhao Y, Yang X, Su B, Zhou C. Blocking the PI3K/AKT and MEK/ERK signaling pathways can overcome gefitinib-resistance in non-small cell lung cancer cell lines. Adv Med Sci. 2011;56:275-284.
28. Rolfo C, Giovannetti E, Hong DS, Bivona T, Raez LE, Bronte G, Buffoni, L, Reguart, N, Santos, ES, Germonpre, P, Taron, M, Passiglia, F, Van Meerbeeck, JP, et al. Novel therapeutic strategies for patients with NSCLC that do not respond to treatment with EGFR inhibitors. Cancer Treat Rev. 2014;40:990-1004.
29. Yang C, Li X, Wang Y, Zhao L, Chen W. Long non-coding RNA UCA1 regulated cell cycle distribution via CREB through PI3-K dependent pathway in bladder carcinoma cells. Gene. 2012;496:8-16.
30. Hampton KK, Craven RJ. Pathways driving the endocytosis of mutant and wild-type EGFR in cancer. Oncoscience. 2014;1:504-512.
31. Wu W, Zhang S, Li X, Xue M, Cao S, Chen W. Ets-2 regulates cell cpoptosis via the Akt pathway,through the regulation of urothelial cancer associated1, a long non-coding RNA, in bladder cancer cells. PLoS One. 2013;8:e73920.
32. Tian Y, Zhang X, Hao Y, Fang Z, He Y. Potential roles of abnormally expressed long noncoding RNA UCA1 and Malat-1 in metastasis of melanoma. Melanoma Res. 2014;24:335-341.
33. Quail DF, Zhang G, Findlay SD, Hess DA, Postovit LM. Nodal promotes invasive phenotypes via a mitogenactivated protein kinase-dependent pathway. Oncogene. 2014;33:461-473.
34. Lee JT. Lessons from X-chromosome inactivation:long ncRNA as guides and tethers to the epigenome. Genes Dev. 2009;23:1831-1842.
35. Li ZK, Li X, Wu SZ, Xue M, Chen W. Long noncoding RNA UCA1 promotes glycolysis by upregulating hexokinase 2 through the mTOR-STAT3/microRNA143 pathway. Cancer Sci. 2014;105:951-955.
36. Niu FY, Wu YL. Novel agents and strategies for overcoming EGFR TKIs resistance. Exp Hematol Oncol. 2014;3:2.
37. Peters S, Zimmermann S, Adjei AA. Oral epidermal growth factor receptor tyrosine kinase inhibitors for the treatment of non-small cell lung cancer:comparative pharmacokinetics and drug-drug interactions. Cancer Treat Rev. 2014;40:917-926.
38. Lee CC, Shiao HY, Wang WC, Hsieh HP. Small-molecule EGFR tyrosine kinase inhibitors for the treatment of cancer. Expert Opin Investig Drugs. 2014;23:1333-1348.
39. Cross DA, Ashton SE, Ghiorghiu S, Eberlein C, Nebhan CA, Spitzler PJ, Orme, J. P, Finlay, M. R, Ward, R. A, Mellor, M. J, Hughes, G, Rahi, A, Jacobs, V. N, et al. AZD9291, an irreversible EGFR TKI, overcomes T790Mmediated resistance to EGFR inhibitors in lung cancer. Cancer Discov. 2014;4:1046-1061.
40. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R, Zeng J, Li M, Fan H, Lin Y, Gu J, Ardayfio O, Zhang J, et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci U S A. 2012;109:21360-21365.
41. Lan W, Zhang D, Jiang J. The roles of LSD1-mediated epigenetic modifications in maintaining the pluripotency of bladder cancer stem cells. Med Hypotheses. 2013;81:823-825.
42. Ding J, Zhang ZM, Xia Y, Liao GQ, Pan Y, Liu S, Zhang Y, Yan ZS. LSD1-mediated epigenetic modification contributes to proliferation and metastasis of colon cancer. Br J Cancer. 2013;109:994-1003.
43. Ju L, Zhou C, Li W, Yan L. Integrin beta1 over-expression associates with resistance to tyrosine kinase inhibitor gefitinib in non-small cell lung cancer. J Cell Biochem. 2010;111:1565-1574.
44. Hirsch FR, Varella-Garcia M, Bunn PA Jr, Di Maria MV, Veve R, Bremmes RM, Barón AE, Zeng C, Franklin WA. Epidermal growth factor receptor in non-small-cell lung carcinomas:correlation between gene copy number and protein expression and impact on prognosis. J Clin Oncol. 2003;21:3798-3807.
45. Pirker R, Pereira JR, von Pawel J, Krzakowski M, Ramlau R, Park K, de Marinis F, Eberhardt WEE, Paz-Ares L, Störkel, S, Schumacher, K-M, von Heydebreck, A, Celik, I, et al. EGFR expression as a predictor of survival for firstline chemotherapy plus cetuximab in patients with advanced non-small-cell lung cancer:analysis of data from the phase 3 FLEX study. Lancet Oncol. 2012;13:33-42.