MiR-222 promotes drug-resistance of breast cancer cells to adriamycin via modulation of PTEN/Akt/FOXO1 pathway

Gene

Volumn 596, Issue , 2017, Pages 110-118

  Shen, Hongyu ^a,b   Wang, Dandan ^b   Li, Liangpeng ^c   Yang, Sujin ^a,b   Chen, Xiu ^a,b   Zhou, Siying ^b,d   Zhong, Shanliang ^b   Zhao, Jianhua ^b   Tang, Jinhai ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b JIANGSU CANCER HOSPITAL   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

^d NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Breast cancer; Drug resistance; miR 222; PTEN Akt FOXO1pathway

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; DOXORUBICIN; MICRORNA 222; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; ANTINEOPLASTIC ANTIBIOTIC; FOXO1 PROTEIN, HUMAN; MICRORNA; MIRN222 MICRORNA, HUMAN; PTEN PROTEIN, HUMAN;

APOPTOSIS ASSAY; ARTICLE; BIOINFORMATICS; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DATA BASE; DRUG SENSITIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IC50; IMMUNOFLUORESCENCE TEST; MCF 7 CELL LINE; MODULATION; MTT ASSAY; OVERALL SURVIVAL; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; METABOLISM; MORTALITY; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; FORKHEAD BOX PROTEIN O1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; MICRORNAS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE;

EID: 84994545584     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2016.10.016     Document Type: Article

References (47)

1. Ahmad, A., Pathways to breast cancer recurrence. ISRN Oncol., 2013, 2013, 290568.
2. Armoni, M., Harel, C., Karni, S., Chen, H., Bar-Yoseph, F., Ver, M.R., Quon, M.J., Karnieli, E., FOXO1 represses peroxisome proliferator-activated receptor-gamma1 and -gamma2 gene promoters in primary adipocytes. A novel paradigm to increase insulin sensitivity. J. Biol. Chem. 281 (2006), 19881–19891.
3. Bar, N., Dikstein, R., miR-22 forms a regulatory loop in PTEN/AKT pathway and modulates signaling kinetics. PLoS One, 5, 2010, e10859.
4. Binkley, J.M., Harris, S.R., Levangie, P.K., Pearl, M., Guglielmino, J., Kraus, V., Rowden, D., Patient perspectives on breast cancer treatment side effects and the prospective surveillance model for physical rehabilitation for women with breast cancer. Cancer 118 (2012), 2207–2216.
5. Boosani, C.S., Agrawal, D.K., PTEN modulators: a patent review. Expert Opin. Ther. Pat. 23 (2013), 569–580.
6. Camp, R.L., Dolled-Filhart, M., Rimm, D.L., X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin. Cancer Res. 10 (2004), 7252–7259.
7. Cancer Genome Atlas, N, Comprehensive molecular portraits of human breast tumours. Nature 490 (2012), 61–70.
8. Carnero, A., Paramio, J.M., The PTEN/PI3K/AKT pathway in vivo, cancer mouse models. Front. Oncol., 4, 2014, 252.
9. Chun-Zhi, Z., Lei, H., An-Ling, Z., Yan-Chao, F., Xiao, Y., Guang-Xiu, W., Zhi-Fan, J., Pei-Yu, P., Qing-Yu, Z., Chun-Sheng, K., MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer, 10, 2010, 367.
10. DeSantis, C.E., Fedewa, S.A., Goding Sauer, A., Kramer, J.L., Smith, R.A., Jemal, A., Breast cancer statistics, 2015: convergence of incidence rates between black and white women. CA Cancer J. Clin. 66 (2016), 31–42.
11. Gan, R., Yang, Y., Yang, X., Zhao, L., Lu, J., Meng, Q.H., Downregulation of miR-221/222 enhances sensitivity of breast cancer cells to tamoxifen through upregulation of TIMP3. Cancer Gene Ther. 21 (2014), 290–296.
12. Gerst, F., Kaiser, G., Panse, M., Sartorius, T., Pujol, A., Hennige, A.M., Machicao, F., Lammers, R., Bosch, F., Haring, H.U., Ullrich, S., Protein kinase Cdelta regulates nuclear export of FOXO1 through phosphorylation of the chaperone 14-3-3zeta. Diabetologia 58 (2015), 2819–2831.
13. Go, H., Jang, J.Y., Kim, P.J., Kim, Y.G., Nam, S.J., Paik, J.H., Kim, T.M., Heo, D.S., Kim, C.W., Jeon, Y.K., MicroRNA-21 plays an oncogenic role by targeting FOXO1 and activating the PI3K/AKT pathway in diffuse large B-cell lymphoma. Oncotarget 6 (2015), 15035–15049.
14. Goto, T., Takano, M., Albergaria, A., Briese, J., Pomeranz, K.M., Cloke, B., Fusi, L., Feroze-Zaidi, F., Maywald, N., Sajin, M., Dina, R.E., Ishihara, O., Takeda, S., Lam, E.W., Bamberger, A.M., Ghaem-Maghami, S., Brosens, J.J., Mechanism and functional consequences of loss of FOXO1 expression in endometrioid endometrial cancer cells. Oncogene 27 (2008), 9–19.
15. Greer, E.L., Brunet, A., FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24 (2005), 7410–7425.
16. Gross, D.N., van den Heuvel, A.P., Birnbaum, M.J., The role of FoxO in the regulation of metabolism. Oncogene 27 (2008), 2320–2336.
17. Guttilla, I.K., White, B.A., Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 284 (2009), 23204–23216.
18. He, L., Hannon, G.J., MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5 (2004), 522–531.
19. Heikkinen, T., Greco, D., Pelttari, L.M., Tommiska, J., Vahteristo, P., Heikkila, P., Blomqvist, C., Aittomaki, K., Nevanlinna, H., Variants on the promoter region of PTEN affect breast cancer progression and patient survival. Breast Cancer Res., 13, 2011, R130.
20. Hoekstra, A.V., Ward, E.C., Hardt, J.L., Lurain, J.R., Singh, D.K., Buttin, B.M., Schink, J.C., Kim, J.J., Chemosensitization of endometrial cancer cells through AKT inhibition involves FOXO1. Gynecol. Oncol. 108 (2008), 609–618.
21. Hou, T., Ou, J., Zhao, X., Huang, X., Huang, Y., Zhang, Y., MicroRNA-196a promotes cervical cancer proliferation through the regulation of FOXO1 and p27Kip1. Br. J. Cancer 110 (2014), 1260–1268.
22. Hu, Q., Gong, J.-P., Li, J., Zhong, S.-L., Chen, W.-X., Zhang, J.-Y., Ma, T.-F., Ji, H., Lv, M.-M., Zhao, J.-H., Tang, J.-H., Down-regulation of miRNA-452 is associated with adriamycin-resistance in breast cancer cells. Asian Pac. J. Cancer Prev. 15 (2014), 5137–5142.
23. Huang, H., Regan, K.M., Wang, F., Wang, D., Smith, D.I., van Deursen, J.M., Tindall, D.J., Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 1649–1654.
24. Kousteni, S., FoxO1: a molecule for all seasons. J. Bone Miner. Res. 26 (2011), 912–917.
25. Kutanzi, K.R., Yurchenko, O.V., Beland, F.A., Checkhun, V.F., Pogribny, I.P., MicroRNA-mediated drug resistance in breast cancer. Clin. Epigenetics 2 (2011), 171–185.
26. Lau, M.T., Klausen, C., Leung, P.C., E-cadherin inhibits tumor cell growth by suppressing PI3K/Akt signaling via beta-catenin-Egr1-mediated PTEN expression. Oncogene 30 (2011), 2753–2766.
27. Liang, R., Rimmele, P., Bigarella, C.L., Yalcin, S., Ghaffari, S., Evidence for AKT-independent regulation of FOXO1 and FOXO3 in haematopoietic stem and progenitor cells. Cell Cycle 15 (2016), 861–867.
28. Liu, P., Cheng, H., Roberts, T.M., Zhao, J.J., Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 8 (2009), 627–644.
29. Magro, G., Righi, A., Casorzo, L., Antonietta, T., Salvatorelli, L., Kacerovska, D., Kazakov, D., Michal, M., Mammary and vaginal myofibroblastomas are genetically related lesions: fluorescence in situ hybridization analysis shows deletion of 13q14 region. Hum. Pathol. 43 (2012), 1887–1893.
30. Majumder, S., Jacob, S.T., Emerging role of microRNAs in drug-resistant breast cancer. Gene Expr. 15 (2011), 141–151.
31. Martin, H.L., Smith, L., Tomlinson, D.C., Multidrug-resistant breast cancer: current perspectives. Breast Cancer (Dove Med Press) 6 (2014), 1–13.
32. Myatt, S.S., Wang, J., Monteiro, L.J., Christian, M., Ho, K.K., Fusi, L., Dina, R.E., Brosens, J.J., Ghaem-Maghami, S., Lam, E.W., Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res. 70 (2010), 367–377.
33. Nakae, J., Oki, M., Cao, Y., The FoxO transcription factors and metabolic regulation. FEBS Lett. 582 (2008), 54–67.
34. O'Driscoll, L., Clynes, M., Biomarkers and multiple drug resistance in breast cancer. Curr. Cancer Drug Targets 6 (2006), 365–384.
35. Rao, X., Di Leva, G., Li, M., Fang, F., Devlin, C., Hartman-Frey, C., Burow, M.E., Ivan, M., Croce, C.M., Nephew, K.P., MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene 30 (2011), 1082–1097.
36. Robertson, N.M., Yigit, M.V., The role of microRNA in resistance to breast cancer therapy. Wiley Interdiscip Rev RNA 5 (2014), 823–833.
37. Sarkar, F.H., Li, Y., Wang, Z., Kong, D., Ali, S., Implication of microRNAs in drug resistance for designing novel cancer therapy. Drug Resist. Updat. 13 (2010), 57–66.
38. Shang, Y., Wang, L.Q., Guo, Q.Y., Shi, T.L., MicroRNA-196a overexpression promotes cell proliferation and inhibits cell apoptosis through PTEN/Akt/FOXO1 pathway. Int. J. Clin. Exp. Pathol. 8 (2015), 2461–2472.
39. Shultz, J.C., Goehe, R.W., Wijesinghe, D.S., Murudkar, C., Hawkins, A.J., Shay, J.W., Minna, J.D., Chalfant, C.E., Alternative splicing of caspase 9 is modulated by the phosphoinositide 3-kinase/Akt pathway via phosphorylation of SRp30a. Cancer Res. 70 (2010), 9185–9196.
40. Siddiqa, A., Long, L.M., Li, L., Marciniak, R.A., Kazhdan, I., Expression of HER-2 in MCF-7 breast cancer cells modulates anti-apoptotic proteins Survivin and Bcl-2 via the extracellular signal-related kinase (ERK) and phosphoinositide-3 kinase (PI3K) signalling pathways. BMC Cancer, 8, 2008, 129.
41. Tang, T., Wong, H.K., Gu, W., Yu, M.Y., To, K.F., Wang, C.C., Wong, Y.F., Cheung, T.H., Chung, T.K., Choy, K.W., MicroRNA-182 plays an onco-miRNA role in cervical cancer. Gynecol. Oncol. 129 (2013), 199–208.
42. Wikman, H., Lamszus, K., Detels, N., Uslar, L., Wrage, M., Benner, C., Hohensee, I., Ylstra, B., Eylmann, K., Zapatka, M., Sauter, G., Kemming, D., Glatzel, M., Muller, V., Westphal, M., Pantel, K., Relevance of PTEN loss in brain metastasis formation in breast cancer patients. Breast Cancer Res., 14, 2012, R49.
43. Wu, L., Li, H., Jia, C.Y., Cheng, W., Yu, M., Peng, M., Zhu, Y., Zhao, Q., Dong, Y.W., Shao, K., Wu, A., Wu, X.Z., MicroRNA-223 regulates FOXO1 expression and cell proliferation. FEBS Lett. 586 (2012), 1038–1043.
44. Wu, Z., He, B., He, J., Mao, X., Upregulation of miR-153 promotes cell proliferation via downregulation of the PTEN tumor suppressor gene in human prostate cancer. Prostate 73 (2013), 596–604.
45. Zeng, L.P., Hu, Z.M., Li, K., Xia, K., miR-222 attenuates cisplatin-induced cell death by targeting the PPP2R2A/Akt/mTOR Axis in bladder cancer cells. J. Cell. Mol. Med. 20 (2016), 559–567.
46. Zhao, L., Ren, Y., Tang, H., Wang, W., He, Q., Sun, J., Zhou, X., Wang, A., Deregulation of the miR-222-ABCG2 regulatory module in tongue squamous cell carcinoma contributes to chemoresistance and enhanced migratory/invasive potential. Oncotarget 6 (2015), 44538–44550.
47. Zhong, S., Li, W., Chen, Z., Xu, J., Zhao, J., MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells. Gene 531 (2013), 8–14.