The role of miR-34 in cancer drug resistance.
RNAi
chemotherapy
drug resistance
miR-34
precision oncology
Journal
Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
20
11
2019
accepted:
31
01
2020
pubmed:
18
2
2020
medline:
5
3
2021
entrez:
18
2
2020
Statut:
ppublish
Résumé
Resistance to conventional chemotherapy remains a major cause of cancer relapse and cancer-related deaths. Therefore, there is an urgent need to overcome resistance barriers. To improve cancer treatment approaches, it is critical to elucidate the basic mechanisms underlying drug resistance. Increasingly, the mechanisms involving micro-RNAs (miRNAs) are studied because miRNAs are also considered practical therapeutic options due to high degrees of specificity, efficacy, and accuracy, as well as their ability to target multiple genes at the same time. Years of research have firmly established miR-34 as a key tumor suppressor miRNA whose target genes are involved in drug resistance mechanisms. Indeed, numerous articles show that low levels of circulating miR-34 or tumor-specific miR-34 expression are associated with poor response to chemotherapy. In addition, elevation of inherently low miR-34 levels in resistant cancer cells effectively restores sensitivity to chemotherapeutic agents. Here, we review this literature, also highlighting some contradictory observations. In addition, we discuss the potential utility of miR-34 expression as a predictive biomarker for chemotherapeutic drug response. Although caution needs to be exercised, miR-34 is emerging as a biomarker that could improve cancer precision medicine.
Substances chimiques
Antineoplastic Agents
0
Biomarkers, Tumor
0
MicroRNAs
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
6424-6440Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Agostini, M., & Knight, R. A. (2014). miR-34: From bench to bedside. Oncotarget, 5(4), 872-881. https://doi.org/10.18632/oncotarget.1825
Aherne, S. T., Madden, S. F., Hughes, D. J., Pardini, B., Naccarati, A., Levy, M., … Clynes, M. (2015). Circulating miRNAs miR-34a and miR-150 associated with colorectal cancer progression. BMC Cancer, 15, 329. https://doi.org/10.1186/s12885-015-1327-5
Akao, Y., Noguchi, S., Iio, A., Kojima, K., Takagi, T., & Naoe, T. (2011). Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Letters, 300(2), 197-204. https://doi.org/10.1016/j.canlet.2010.10.006
Bader, A. G. (2012). miR-34-a microRNA replacement therapy is headed to the clinic. Frontiers in Genetics, 3, 120. https://doi.org/10.3389/fgene.2012.00120
Beg, M. S., Brenner, A. J., Sachdev, J., Borad, M., Kang, Y. K., Stoudemire, J., … Hong, D. S. (2017). Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Investigational New Drugs, 35(2), 180-188. https://doi.org/10.1007/s10637-016-0407-y
Cao, W., Yang, W., Fan, R., Li, H., Jiang, J., Geng, M., … Wu, Y. (2014). miR-34a regulates cisplatin-induce gastric cancer cell death by modulating PI3K/AKT/survivin pathway. Tumour Biology, 35(2), 1287-1295. https://doi.org/10.1007/s13277-013-1171-7
Chen, X., Peng, D., Shen, Y., Liu, B., Zhou, H., Tao, H., & Huang, J. (2017). The potential combinational effect of miR-34a with celecoxib in osteosarcoma. Anti-Cancer Drugs, 28(8), 888-897. https://doi.org/10.1097/cad.0000000000000530
Cheng, C., Qin, Y., Zhi, Q., Wang, J., & Qin, C. (2018). Knockdown of long non-coding RNA HOTAIR inhibits cisplatin resistance of gastric cancer cells through inhibiting the PI3K/Akt and Wnt/beta-catenin signaling pathways by up-regulating miR-34a. International Journal of Biological Macromolecules, 107(Pt B), 2620-2629. https://doi.org/10.1016/j.ijbiomac.2017.10.154
Corcoran, C., Rani, S., & O'Driscoll, L. (2014). miR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression. Prostate, 74(13), 1320-1334. https://doi.org/10.1002/pros.22848
Deng, X., Cao, M., Zhang, J., Hu, K., Yin, Z., Zhou, Z., … Zeng, Y. (2014). Hyaluronic acid-chitosan nanoparticles for co-delivery of miR-34a and doxorubicin in therapy against triple negative breast cancer. Biomaterials, 35(14), 4333-4344. https://doi.org/10.1016/j.biomaterials.2014.02.006
Eichelser, C., Flesch-Janys, D., Chang-Claude, J., Pantel, K., & Schwarzenbach, H. (2013). Deregulated serum concentrations of circulating cell-free microRNAs miR-17, miR-34a, miR-155, and miR-373 in human breast cancer development and progression. Clinical Chemistry, 59(10), 1489-1496. https://doi.org/10.1373/clinchem.2013.205161
Fadejeva, I., Olschewski, H., & Hrzenjak, A. (2017). microRNAs as regulators of cisplatin-resistance in non-small cell lung carcinomas. Oncotarget, 8(70), 115754-115773. https://doi.org/10.18632/oncotarget.22975
Fan, Y. N., Meley, D., Pizer, B., & See, V. (2014). miR-34a mimics are potential therapeutic agents for p53-mutated and chemo-resistant brain tumour cells. PLOS One, 9(9):e108514. https://doi.org/10.1371/journal.pone.0108514
Farooqi, A. A., Tabassum, S., & Ahmad, A. (2017). MicroRNA-34a: A versatile regulator of myriads of targets in different cancers. International Journal of Molecular Sciences, 18(10), 2089. https://doi.org/10.3390/ijms18102089
Franchina, T., Amodeo, V., Bronte, G., Savio, G., Ricciardi, G. R., Picciotto, M., … Adamo, V. (2014). Circulating miR-22, miR-24 and miR-34a as novel predictive biomarkers to pemetrexed-based chemotherapy in advanced non-small cell lung cancer. Journal of Cellular Physiology, 229(1), 97-99. https://doi.org/10.1002/jcp.24422
Freres, P., Josse, C., Bovy, N., Boukerroucha, M., Struman, I., Bours, V., & Jerusalem, G. (2015). Neoadjuvant chemotherapy in breast cancer patients induces miR-34a and miR-122 expression. Journal of Cellular Physiology, 230(2), 473-481. https://doi.org/10.1002/jcp.24730
Freres, P., Wenric, S., Boukerroucha, M., Fasquelle, C., Thiry, J., Bovy, N., … Jerusalem, G. (2016). Circulating microRNA-based screening tool for breast cancer. Oncotarget, 7(5), 5416-5428. https://doi.org/10.18632/oncotarget.6786
Fu, Y., Li, C., Luo, Y., Li, L., Liu, J., & Gui, R. (2018). Silencing of long non-coding RNA MIAT sensitizes lung cancer cells to gefitinib by epigenetically regulating miR-34a. Frontiers in Pharmacology, 9, 82. https://doi.org/10.3389/fphar.2018.00082
Fujita, Y., Kojima, K., Hamada, N., Ohhashi, R., Akao, Y., Nozawa, Y., … Ito, M. (2008). Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochemical and Biophysical Research Communications, 377(1), 114-119. https://doi.org/10.1016/j.bbrc.2008.09.086
Garajova, I., Le Large, T. Y., Frampton, A. E., Rolfo, C., Voortman, J., & Giovannetti, E. (2014). Molecular mechanisms underlying the role of microRNAs in the chemoresistance of pancreatic cancer. BioMed Research International, 2014, 678401-678417. https://doi.org/10.1155/2014/678401
Gong, L. G., Shi, J. C., Shang, J., Hao, J. G., & Du, X. (2019). Effect of miR-34a on resistance to sunitinib in breast cancer by regulating the Wnt/beta-catenin signaling pathway. European Review for Medical and Pharmacological Sciences, 23(3), 1151-1157. https://doi.org/10.26355/eurrev_201902_17006
Hamam, R., Hamam, D., Alsaleh, K. A., Kassem, M., Zaher, W., Alfayez, M., … Alajez, N. M. (2017). Circulating microRNAs in breast cancer: Novel diagnostic and prognostic biomarkers. Cell Death & Disease, 8(9):e3045. https://doi.org/10.1038/cddis.2017.440
Hayes, J., Peruzzi, P. P., & Lawler, S. (2014). MicroRNAs in cancer: Biomarkers, functions and therapy. Trends in Molecular Medicine, 20(8), 460-469. https://doi.org/10.1016/j.molmed.2014.06.005
Hummel, R., Hussey, D. J., & Haier, J. (2010). microRNAs: Predictors and modifiers of chemo- and radiotherapy in different tumour types. European Journal of Cancer, 46(2), 298-311. https://doi.org/10.1016/j.ejca.2009.10.027
Imani, S., Wu, R. C., & Fu, J. (2018). MicroRNA-34 family in breast cancer: From research to therapeutic potential. Journal of Cancer, 9(20), 3765-3775. https://doi.org/10.7150/jca.25576
Imani, S., Zhang, X., Hosseinifard, H., Fu, S., & Fu, J. (2017). The diagnostic role of microRNA-34a in breast cancer: A systematic review and meta-analysis. Oncotarget, 8(14), 23177-23187. https://doi.org/10.18632/oncotarget.15520
Ji, Q., Hao, X., Meng, Y., Zhang, M., Desano, J., Fan, D., & Xu, L. (2008). Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer, 8, 266. https://doi.org/10.1186/1471-2407-8-266
Ji, Q., Hao, X., Zhang, M., Tang, W., Yang, M., Li, L., … Xu, L. (2009). microRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLOS One, 4(8):e6816. https://doi.org/10.1371/journal.pone.0006816
Ji, X., Wang, Z., Geamanu, A., Goja, A., Sarkar, F. H., & Gupta, S. V. (2012). Delta-tocotrienol suppresses Notch-1 pathway by upregulating miR-34a in nonsmall cell lung cancer cells. International Journal of Cancer, 131(11), 2668-2677. https://doi.org/10.1002/ijc.27549
Jian, C., Tu, M. J., Ho, P. Y., Duan, Z., Zhang, Q., Qiu, J. X., … Yu, A. M. (2017). Co-targeting of DNA, RNA, and protein molecules provides optimal outcomes for treating osteosarcoma and pulmonary metastasis in spontaneous and experimental metastasis mouse models. Oncotarget, 8(19), 30742-30755. https://doi.org/10.18632/oncotarget.16372
Juracek, J., Stanik, M., Vesela, P., Radova, L., Dolezel, J., Svoboda, M., & Slaby, O. (2019). Tumor expression of miR-34a-3p is an independent predictor of recurrence in non-muscle-invasive bladder cancer and promising additional factor to improve predictive value of EORTC nomogram. Urologic Oncology, 37(3), 184. https://doi.org/10.1016/j.urolonc.2018.10.014
Kang, L., Mao, J., Tao, Y., Song, B., Ma, W., Lu, Y., … Li, L. (2015). MicroRNA-34a suppresses the breast cancer stem cell-like characteristics by downregulating Notch1 pathway. Cancer Prevention Research, 106(6), 700-708. https://doi.org/10.1111/cas.12656
Kasinski, A. L., Kelnar, K., Stahlhut, C., Orellana, E., Zhao, J., Shimer, E., … Slack, F. J. (2015). A combinatorial microRNA therapeutics approach to suppressing non-small cell lung cancer. Oncogene, 34(27), 3547-3555. https://doi.org/10.1038/onc.2014.282
Kastl, L., Brown, I., & Schofield, A. C. (2012). miRNA-34a is associated with docetaxel resistance in human breast cancer cells. Breast Cancer Research and Treatment, 131(2), 445-454. https://doi.org/10.1007/s10549-011-1424-3
Kim, C. H., Kim, H. K., Rettig, R. L., Kim, J., Lee, E. T., Aprelikova, O., … Green, J. E. (2011). miRNA signature associated with outcome of gastric cancer patients following chemotherapy. BMC Medical Genomics, 4, 79. https://doi.org/10.1186/1755-8794-4-79
Kim do, Y., Park, E. Y., Chang, E., Kang, H. G., Koo, Y., Lee, E. J., … Park, J. H. (2016). A novel miR-34a target, protein kinase D1, stimulates cancer stemness and drug resistance through GSK3/beta-catenin signaling in breast cancer. Oncotarget, 7(12), 14791-14802. https://doi.org/10.18632/oncotarget.7443
Kojima, K., Fujita, Y., Nozawa, Y., Deguchi, T., & Ito, M. (2010). miR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate, 70(14), 1501-1512. https://doi.org/10.1002/pros.21185
Lai, M., Du, G., Shi, R., Yao, J., Yang, G., Wei, Y., … Wang, L. (2015). miR-34a inhibits migration and invasion by regulating the SIRT1/p53 pathway in human SW480 cells. Molecular Medicine Reports, 11(5), 3301-3307. https://doi.org/10.3892/mmr.2015.3182
Li, H., Rokavec, M., Jiang, L., Horst, D., & Hermeking, H. (2017). Antagonistic effects of p53 and HIF1A on microRNA-34a regulation of PPP1R11 and STAT3 and hypoxia-induced Epithelial to mesenchymal transition in colorectal cancer cells. Gastroenterology, 153(2), 505-520. https://doi.org/10.1053/j.gastro.2017.04.017
Li, H., Yu, G., Shi, R., Lang, B., Chen, X., Xia, D., … Xu, H. (2014). Cisplatin-induced epigenetic activation of miR-34a sensitizes bladder cancer cells to chemotherapy. Molecular Cancer, 13, 8. https://doi.org/10.1186/1476-4598-13-8
Li, L., Yuan, L., Luo, J., Gao, J., Guo, J., & Xie, X. (2013). miR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clinical and Experimental Medicine, 13(2), 109-117. https://doi.org/10.1007/s10238-012-0186-5
Li, Q. C., Xu, H., Wang, X., Wang, T., & Wu, J. (2017). miR-34a increases cisplatin sensitivity of osteosarcoma cells in vitro through up-regulation of c-Myc and Bim signal. Cancer Biomarkers: Section A of Disease Markers, 21(1), 135-144. https://doi.org/10.3233/cbm-170452
Li, X., Zhao, H., Zhou, X., & Song, L. (2015). Inhibition of lactate dehydrogenase A by microRNA-34a resensitizes colon cancer cells to 5-fluorouracil. Molecular Medicine Reports, 11(1), 577-582. https://doi.org/10.3892/mmr.2014.2726
Li, X. J., Ji, M. H., Zhong, S. L., Zha, Q. B., Xu, J. J., Zhao, J. H., & Tang, J. H. (2012). microRNA-34a modulates chemosensitivity of breast cancer cells to adriamycin by targeting Notch1. Archives of Medical Research, 43(7), 514-521. https://doi.org/10.1016/j.arcmed.2012.09.007
Li, Y., Gong, P., Hou, J. X., Huang, W., Ma, X. P., Wang, Y. L., … Li, N. (2018). miR-34a regulates multidrug resistance via positively modulating OAZ2 signaling in colon cancer cells. Journal of Immunology Research, 2018, 7498514-13. https://doi.org/10.1155/2018/7498514
Lin, F., Wen, D., Wang, X., & Mahato, R. I. (2019). Dual responsive micelles capable of modulating miRNA-34a to combat taxane resistance in prostate cancer. Biomaterials, 192, 95-108. https://doi.org/10.1016/j.biomaterials.2018.10.036
Lin, X., Chen, W., Wei, F., Zhou, B. P., Hung, M. C., & Xie, X. (2017). Nanoparticle delivery of miR-34a eradicates long-term-cultured breast cancer stem cells via targeting C22ORF28 directly. Theranostics, 7(19), 4805-4824. https://doi.org/10.7150/thno.20771
Liu, B., Su, F., Li, Y., Qi, X., Liu, X., Liang, W., … Zhang, J. (2017). Changes of serum miR34a expression during neoadjuvant chemotherapy predict the treatment response and prognosis in stage II/III breast cancer. Biomedicine and Pharmacotherapy, 88, 911-917. https://doi.org/10.1016/j.biopha.2017.01.133
Liu, K., Huang, J., Xie, M., Yu, Y., Zhu, S., Kang, R., … Duan, X. (2014). MIR34A regulates autophagy and apoptosis by targeting HMGB1 in the retinoblastoma cell. Autophagy, 10(3), 442-452. https://doi.org/10.4161/auto.27418
Liu, X., Liu, X., Wu, Y., Fang, Z., Wu, Q., Wu, C., … Li, L. (2018). MicroRNA-34a attenuates metastasis and chemoresistance of bladder cancer cells by targeting the TCF1/LEF1 axis. Cellular Physiology and Biochemistry, 48(1), 87-98. https://doi.org/10.1159/000491665
Liu, X., Luo, X., Wu, Y., Xia, D., Chen, W., Fang, Z., … Li, L. (2018). microRNA-34a attenuates paclitaxel resistance in prostate cancer cells via direct suppression of JAG1/Notch1 axis. Cellular Physiology and Biochemistry, 50(1), 261-276. https://doi.org/10.1159/000494004
Lv, T., Song, K., Zhang, L., Li, W., Chen, Y., Diao, Y., … Liu, P. (2018). miRNA-34a decreases ovarian cancer cell proliferation and chemoresistance by targeting HDAC1. Biochemistry and Cell Biology, 96(5), 663-671. https://doi.org/10.1139/bcb-2018-0031
Ma, W., Xiao, G. G., Mao, J., Lu, Y., Song, B., Wang, L., … Li, L. (2015). Dysregulation of the miR-34a-SIRT1 axis inhibits breast cancer stemness. Oncotarget, 6(12), 10432-10444. https://doi.org/10.18632/oncotarget.3394
Marques, S. C., Ranjbar, B., Laursen, M. B., Falgreen, S., Bilgrau, A. E., Bodker, J. S., … Dybkaer, K. (2016). High miR-34a expression improves response to doxorubicin in diffuse large B-cell lymphoma. Experimental Hematology, 44(4), 238-246. https://doi.org/10.1016/j.exphem.2015.12.007
Momtazi, A. A., Shahabipour, F., Khatibi, S., Johnston, T. P., Pirro, M., & Sahebkar, A. (2016). Curcumin as a microRNA regulator in cancer: A review. Reviews of Physiology Biochemistry and Pharmacology, 171, 1-38. https://doi.org/10.1007/112_2016_3
Nakatani, F., Ferracin, M., Manara, M. C., Ventura, S., Del Monaco, V., Ferrari, S., … Scotlandi, K. (2012). miR-34a predicts survival of Ewing's sarcoma patients and directly influences cell chemo-sensitivity and malignancy. Journal of Pathology, 226(5), 796-805. https://doi.org/10.1002/path.3007
O'Brien, K. P., Ramphul, E., Howard, L., Gallagher, W. M., Malone, C., Kerin, M. J., & Dwyer, R. M. (2017). Circulating microRNAs in cancer. Methods in Molecular Biology, 1509, 123-139. https://doi.org/10.1007/978-1-4939-6524-3_12
Park, E. Y., Chang, E., Lee, E. J., Lee, H. W., Kang, H. G., Chun, K. H., … Park, J. H. (2014). Targeting of miR34a-NOTCH1 axis reduced breast cancer stemness and chemoresistance. Cancer Research, 74(24), 7573-7582. https://doi.org/10.1158/0008-5472.Can-14-1140
Pu, Y., Zhao, F., Li, Y., Cui, M., Wang, H., Meng, X., & Cai, S. (2017). The miR-34a-5p promotes the multi-chemoresistance of osteosarcoma via repression of the AGTR1 gene. BMC Cancer, 17(1), 45. https://doi.org/10.1186/s12885-016-3002-x
Pu, Y., Zhao, F., Wang, H., & Cai, S. (2017). miR-34a-5p promotes multi-chemoresistance of osteosarcoma through down-regulation of the DLL1 gene. Scientific Reports, 7, 44218. https://doi.org/10.1038/srep44218
Pu, Y., Zhao, F., Wang, H., Cai, W., Gao, J., Li, Y., & Cai, S. (2016). miR-34a-5p promotes the multi-drug resistance of osteosarcoma by targeting the CD117 gene. Oncotarget, 7(19), 28420-28434. https://doi.org/10.18632/oncotarget.8546
Riquelme, I., Letelier, P., Riffo-Campos, A. L., Brebi, P., & Roa, J. C. (2016). Emerging role of miRNAs in the drug resistance of gastric cancer. International Journal of Molecular Sciences, 17(3), 424. https://doi.org/10.3390/ijms17030424
Rokavec, M., Oner, M. G., Li, H., Jackstadt, R., Jiang, L., Lodygin, D., … Hermeking, H. (2014). IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. Journal of Clinical Investigation, 124(4), 1853-1867. https://doi.org/10.1172/jci73531
Van Roosbroeck, K., & Calin, G. A. (2017). Cancer hallmarks and microRNAs: The therapeutic connection. Advances in Cancer Research, 135, 119-149. https://doi.org/10.1016/bs.acr.2017.06.002
Shi, S., Han, L., Deng, L., Zhang, Y., Shen, H., Gong, T., … Sun, X. (2014). Dual drugs (microRNA-34a and paclitaxel)-loaded functional solid lipid nanoparticles for synergistic cancer cell suppression. Journal of Controlled Release, 194, 228-237. https://doi.org/10.1016/j.jconrel.2014.09.005
Siegel, R. L., Miller, K. D., & Jemal, A. (2019). Cancer statistics, 2019. CA: A Cancer Journal for Clinicians, 69(1), 7-34. https://doi.org/10.3322/caac.21551
Siemens, H., Jackstadt, R., Kaller, M., & Hermeking, H. (2013). Repression of c-Kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget, 4(9), 1399-1415. https://doi.org/10.18632/oncotarget.1202
Slabakova, E., Culig, Z., Remsik, J., & Soucek, K. (2017). Alternative mechanisms of miR-34a regulation in cancer. Cell Death & Disease, 8(10):e3100. https://doi.org/10.1038/cddis.2017.495
Soltani-Sedeh, H., Irani, S., Mirfakhraie, R., & Soleimani, M. (2019). Potential using of microRNA-34A in combination with paclitaxel in colorectal cancer cells. Journal of Cancer Research and Therapeutics, 15(1), 32-37. https://doi.org/10.4103/jcrt.JCRT_267_17
Song, C., Lu, P., Sun, G., Yang, L., Wang, Z., & Wang, Z. (2017). miR-34a sensitizes lung cancer cells to cisplatin via p53/miR-34a/MYCN axis. Biochemical and Biophysical Research Communications, 482(1), 22-27. https://doi.org/10.1016/j.bbrc.2016.11.037
Stahlhut, C., & Slack, F. J. (2015). Combinatorial action of microRNAs let-7 and miR-34 effectively synergizes with erlotinib to suppress non-small cell lung cancer cell proliferation. Cell Cycle, 14(13), 2171-2180. https://doi.org/10.1080/15384101.2014.1003008
Sudhakar, A. (2009). History of cancer, ancient and modern treatment methods. Journal of Cancer Science and Therapy, 1(2), 1-4. https://doi.org/10.4172/1948-5956.100000e2
Sun, C., Wang, F. J., Zhang, H. G., Xu, X. Z., Jia, R. C., Yao, L., & Qiao, P. F. (2017). miR-34a mediates oxaliplatin resistance of colorectal cancer cells by inhibiting macroautophagy via transforming growth factor-beta/Smad4 pathway. World Journal of Gastroenterology, 23(10), 1816-1827. https://doi.org/10.3748/wjg.v23.i10.1816
Vinall, R. L., Ripoll, A. Z., Wang, S., Pan, C. X., & deVere White, R. W. (2012). miR-34a chemosensitizes bladder cancer cells to cisplatin treatment regardless of p53-Rb pathway status. International Journal of Cancer, 130(11), 2526-2538. https://doi.org/10.1002/ijc.26256
Wang, X., Dong, K., Gao, P., Long, M., Lin, F., Weng, Y., … Zhang, H. (2013). microRNA-34a sensitizes lung cancer cell lines to DDP treatment independent of p53 status. Cancer Biotherapy and Radiopharmaceuticals, 28(1), 45-50. https://doi.org/10.1089/cbr.2012.1218
Wang, Y., Chen, J., Liang, X., Han, H., Wang, H., Yang, Y., & Li, Q. (2017). An ATP-responsive codelivery system of doxorubicin and miR-34a to synergistically inhibit cell proliferation and migration. Molecular pharmaceutics, 14(7), 2323-2332. https://doi.org/10.1021/acs.molpharmaceut.7b00184
Wang, Y., & Wang, L. (2017). miR-34a attenuates glioma cells progression and chemoresistance via targeting PD-L1. Biotechnology Letters, 39(10), 1485-1492. https://doi.org/10.1007/s10529-017-2397-z
Weeraratne, S. D., Amani, V., Neiss, A., Teider, N., Scott, D. K., Pomeroy, S. L., & Cho, Y. J. (2011). miR-34a confers chemosensitivity through modulation of MAGE-A and p53 in medulloblastoma. Neuro-oncology, 13(2), 165-175. https://doi.org/10.1093/neuonc/noq179
Wen, D., Peng, Y., Lin, F., Singh, R. K., & Mahato, R. I. (2017). Micellar delivery of miR-34a modulator rubone and paclitaxel in resistant prostate cancer. Cancer Research, 77(12), 3244-3254. https://doi.org/10.1158/0008-5472.Can-16-2355
Wu, H., Huang, M., Lu, M., Zhu, W., Shu, Y., Cao, P., & Liu, P. (2013). Regulation of microtubule-associated protein tau (MAPT) by miR-34c-5p determines the chemosensitivity of gastric cancer to paclitaxel. Cancer Chemotherapy and Pharmacology, 71(5), 1159-1171. https://doi.org/10.1007/s00280-013-2108-y
Wu, M. Y., Fu, J., Xiao, X., Wu, J., & Wu, R. C. (2014). miR-34a regulates therapy resistance by targeting HDAC1 and HDAC7 in breast cancer. Cancer Letters, 354(2), 311-319. https://doi.org/10.1016/j.canlet.2014.08.031
Wu, Y., Dai, X., Ni, Z., Yan, X., He, F., & Lian, J. (2017). The downregulation of ATG4B mediated by microRNA-34a/34c-5p suppresses rapamycin-induced autophagy. Iranian Journal of Basic Medical Sciences, 20(10), 1125-1130. https://doi.org/10.22038/ijbms.2017.9446
Xin, Y., Huang, M., Guo, W. W., Huang, Q., Zhang, L. Z., & Jiang, G. (2017). Nano-based delivery of RNAi in cancer therapy. Molecular Cancer, 16(1), 134. https://doi.org/10.1186/s12943-017-0683-y
Xue, W., Dahlman, J. E., Tammela, T., Khan, O. F., Sood, S., Dave, A., … Jacks, T. (2014). Small RNA combination therapy for lung cancer. Proceedings of the National Academy of Sciences of the United States of America, 111(34), E3553-E3561. https://doi.org/10.1073/pnas.1412686111
Yang, F., Li, Q. J., Gong, Z. B., Zhou, L., You, N., Wang, S., … Dou, K. F. (2014). microRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technology in Cancer Research & Treatment, 13(1), 77-86. https://doi.org/10.7785/tcrt.2012.500364
Yao, C., Liu, J., Wu, X., Tai, Z., Gao, Y., Zhu, Q., … Gao, S. (2016). Reducible self-assembling cationic polypeptide-based micelles mediate co-delivery of doxorubicin and microRNA-34a for androgen-independent prostate cancer therapy. Journal of Controlled Release, 232, 203-214. https://doi.org/10.1016/j.jconrel.2016.04.034
You, L., Shou, J., Deng, D., Jiang, L., Jing, Z., Yao, J., … Han, W. (2015). Crizotinib induces autophagy through inhibition of the STAT3 pathway in multiple lung cancer cell lines. Oncotarget, 6(37), 40268-40282. https://doi.org/10.18632/oncotarget.5592
Yu, G., Yao, W., Xiao, W., Li, H., Xu, H., & Lang, B. (2014). microRNA-34a functions as an anti-metastatic microRNA and suppresses angiogenesis in bladder cancer by directly targeting CD44. Journal of Experimental & Clinical Cancer Research, 33, 779. https://doi.org/10.1186/s13046-014-0115-4
Yu, G., Zhong, N., Chen, G., Huang, B., & Wu, S. (2014). Downregulation of PEBP4, a target of miR-34a, sensitizes drug-resistant lung cancer cells. Tumour Biology, 35(10), 10341-10349. https://doi.org/10.1007/s13277-014-2284-3
Yun, M. R., Lim, S. M., Kim, S. K., Choi, H. M., Pyo, K. H., Kim, S. K., … Cho, B. C. (2018). Enhancer remodeling and microRNA alterations are associated with acquired resistance to ALK inhibitors. Cancer Research, 78(12), 3350-3362. https://doi.org/10.1158/0008-5472.Can-17-3146
Zenz, T., Mohr, J., Eldering, E., Kater, A. P., Buhler, A., Kienle, D., … Stilgenbauer, S. (2009). miR-34a as part of the resistance network in chronic lymphocytic leukemia. Blood, 113(16), 3801-3808. https://doi.org/10.1182/blood-2008-08-172254
Zhang, G., Tian, X., Li, Y., Wang, Z., Li, X., & Zhu, C. (2018). miR-27b and miR-34a enhance docetaxel sensitivity of prostate cancer cells through inhibiting epithelial-to-mesenchymal transition by targeting ZEB1. Biomedicine and Pharmacotherapy, 97, 736-744. https://doi.org/10.1016/j.biopha.2017.10.163
Zhang, L., Yang, X., Lv, Y., Xin, X., Qin, C., Han, X., … Yin, L. (2017). Cytosolic co-delivery of miRNA-34a and docetaxel with core-shell nanocarriers via caveolae-mediated pathway for the treatment of metastatic breast cancer. Scientific Reports, 7, 46186. https://doi.org/10.1038/srep46186
Zhang, Q., Wang, J., Li, N., Liu, Z., Chen, Z., Li, Z., … Gao, J. (2018). miR-34a increases the sensitivity of colorectal cancer cells to 5-fluorouracil in vitro and in vivo. American Journal of Cancer Research, 8(2), 280-290.
Zhang, Q. A., Yang, X. H., Chen, D., Yan, X., Jing, F. C., Liu, H. Q., & Zhang, R. (2018). miR-34 increases in vitro PANC-1 cell sensitivity to gemcitabine via targeting Slug/PUMA. Cancer Biomarkers: Section A of Disease Markers, 21(4), 755-762. https://doi.org/10.3233/cbm-170289
Zhang, Z., Kong, Y., Yang, W., Ma, F., Zhang, Y., Ji, S., … Hua, Y. (2016). Upregulation of microRNA-34a enhances the DDP sensitivity of gastric cancer cells by modulating proliferation and apoptosis via targeting MET. Oncology Reports, 36(4), 2391-2397. https://doi.org/10.3892/or.2016.5016
Zhao, J., Guerrero, A., Kelnar, K., Peltier, H. J., & Bader, A. G. (2017). Synergy between next generation EGFR tyrosine kinase inhibitors and miR-34a in the inhibition of non-small cell lung cancer. Lung Cancer, 108, 96-102. https://doi.org/10.1016/j.lungcan.2017.02.020
Zhao, J., Kelnar, K., & Bader, A. G. (2014). In-depth analysis shows synergy between erlotinib and miR-34a. PLOS One, 9(2):e89105. https://doi.org/10.1371/journal.pone.0089105
Zhao, K., Cheng, J., Chen, B., Liu, Q., Xu, D., & Zhang, Y. (2017). Circulating microRNA-34 family low expression correlates with poor prognosis in patients with non-small cell lung cancer. Journal of Thoracic Disease, 9(10), 3735-3746. https://doi.org/10.21037/jtd.2017.09.01
Zhao, Y., Tu, M. J., Yu, Y. F., Wang, W. P., Chen, Q. X., Qiu, J. X., … Yu, A. M. (2015). Combination therapy with bioengineered miR-34a prodrug and doxorubicin synergistically suppresses osteosarcoma growth. Biochemical Pharmacology, 98(4), 602-613. https://doi.org/10.1016/j.bcp.2015.10.015
Zhou, J. Y., Chen, X., Zhao, J., Bao, Z., Chen, X., Zhang, P., … Zhou, J. Y. (2014). microRNA-34a overcomes HGF-mediated gefitinib resistance in EGFR mutant lung cancer cells partly by targeting MET. Cancer Letters, 351(2), 265-271. https://doi.org/10.1016/j.canlet.2014.06.010
Zhou, Y., Zhao, R. H., Tseng, K. F., Li, K. P., Lu, Z. G., Liu, Y., … Min, D. L. (2016). Sirolimus induces apoptosis and reverses multidrug resistance in human osteosarcoma cells in vitro via increasing microRNA-34b expression. Acta Pharmacologica Sinica, 37(4), 519-529. https://doi.org/10.1038/aps.2015.153