MiR-200c inhibits autophagy and enhances radiosensitivity in breast cancer cells by targeting UBQLN1

International Journal of Cancer

Volumn 136, Issue 5, 2015, Pages 1003-1012

  Sun, Quanquan ^a   Liu, Tongxin ^a   Yuan, Yawei ^a   Guo, Zhenli ^b   Xie, Guozhu ^a   Du, Shasha ^a   Lin, Xiaoshan ^a   Xu, Zhixin ^a   Liu, Minfeng ^a   Wang, Wei ^a   Yuan, Quan ^c   Chen, Longhua ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c JULES STEIN EYE INSTITUTE   (United States)

Author keywords

Autophagy; Breast cancer; miR 200c; Radioresistance; UBQLN1

Indexed keywords

MICRORNA 200C; PEPTIDES AND PROTEINS; UBIQUILIN 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; CELL CYCLE PROTEIN; LIGHT CHAIN 3, HUMAN; LUCIFERASE; MESSENGER RNA; MICRORNA; MICROTUBULE ASSOCIATED PROTEIN; MIRN200 MICRORNA, HUMAN; SMALL INTERFERING RNA; UBQLN1 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGY; BREAST CANCER; BREAST CANCER CELL LINE; BT474 CELL LINE; BT549 CELL LINE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MCF 7 CELL LINE; MDA MB 231 CELL LINE; PROTEIN EXPRESSION; PROTEIN TARGETING; RADIOSENSITIVITY; RNA ANALYSIS; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BREAST; BREAST NEOPLASMS; CARCINOMA, BASAL CELL; CELL CULTURE; CELL PROLIFERATION; ENZYME IMMUNOASSAY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PATHOLOGY; RADIATION DOSE; RADIATION RESPONSE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; BREAST; BREAST NEOPLASMS; CARCINOMA, BASAL CELL; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION; LUCIFERASES; MICRORNAS; MICROTUBULE-ASSOCIATED PROTEINS; RADIATION TOLERANCE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84918810610     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29065     Document Type: Article

References (47)

1. Parkin DM, Bray F, Ferlay J, et al. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
2. Darby S, McGale P, Correa C, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10, 801 women in 17 randomised trials. Lancet 2011;378:1707-16.
3. Voduc KD, Cheang MC, Tyldesley S, et al. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 2010;28:1684-91.
4. Nguyen PL, Taghian AG, Katz MS, et al. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol 2008;26:2373-8.
5. Kyndi M, Sorensen FB, Knudsen H, et al. Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in highrisk breast cancer: the Danish Breast Cancer Cooperative Group. J Clin Oncol 2008;26:1419-26.
6. Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-75.
7. Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 2013;368:651-62.
8. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008;132:27-42.
9. Ravikumar B, Sarkar S, Davies JE, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010;90:1383-435.
10. Wang P, Zhang J, Zhang L, et al. MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology 2013;145:1133-43.
11. Chang Y, Yan W, He X, et al. miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology 2012;143:177-87.
12. McAlpine F, Williamson LE, Tooze SA, et al. Regulation of nutrient-sensitive autophagy by uncoordinated 51-like kinases 1 and 2. Autophagy 2013;9:361-73.
13. Yu Y, Yang L, Zhao M, et al. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells. Leukemia 2012;26:1752-60.
14. Croce CM. Causes and consequences of micro-RNA dysregulation in cancer. Nat Rev Genet 2009;10:704-14.
15. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 2009;27:5848-56.
16. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-66.
17. Tekirdag KA, Korkmaz G, Ozturk DG, et al. MIR181A regulates starvation- and rapamycininduced autophagy through targeting of ATG5. Autophagy 2013;9:374-85.
18. Shimono Y, Zabala M, Cho RW, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 2009;138:592-603.
19. Jurmeister S, Baumann M, Balwierz A, et al. MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol Cell Biol 2012;32:633-51.
20. Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
21. Cochrane DR, Howe EN, Spoelstra NS, et al. Loss of miR-200c: a marker of aggressiveness and chemoresistance in female reproductive cancers. J Oncol 2010;2010:821717.
22. Park SM, Gaur AB, Lengyel E, 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;22:894-907.
23. Hurteau GJ, Carlson JA, Roos E, et al. Stable expression of miR-200c alone is sufficient to regulate TCF8 (ZEB1) and restore E-cadherin expression. Cell Cycle 2009;8:2064-9.
24. Lin J, Liu C, Gao F, et al. miR-200c enhances radiosensitivity of human breast cancer cells. J Cell Biochem 2013;114:606-15.
25. Shi L, Zhang S, Wu H, et al. MiR-200c increases the radiosensitivity of non-small-cell lung cancer cell line A549 by targeting VEGF-VEGFR2 pathway. PLoS One 2013;8:e78344.
26. Xie G, Zhan J, Tian Y, et al. Mammosphere cells from high-passage MCF7 cell line show variable loss of tumorigenicity and radioresistance. Cancer Lett 2012;316:53-61.
27. Yano S, Wang W, Li Q, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptoractivating mutations. Cancer Res 2008;68:9479-87.
28. Cochrane DR, Spoelstra NS, Howe EN, et al. MicroRNA-200c mitigates invasiveness and restores sensitivity to microtubule-targeting chemotherapeutic agents. Mol Cancer Ther 2009;8:1055-66.
29. Bristol ML, Di X, Beckman MJ, et al. Dual functions of autophagy in the response of breast tumor cells to radiation: cytoprotective autophagy with radiation alone and cytotoxic autophagy in radiosensitization by vitamin D 3. Autophagy 2012;8:739-53.
30. Mazure NM, Pouyssegur J. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol 2010;22:177-80.
31. Apel A, Herr I, Schwarz H, et al. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 2008;68:1485-94.
32. Devarajan E, Sahin AA, Chen JS, et al. Downregulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene 2002;21:8843-51.
33. Rothenberg C, Srinivasan D, Mah L, et al. Ubiquilin functions in autophagy and is degraded by chaperone-mediated autophagy. Hum Mol Genet 2010;19:3219-32.
34. Beverly LJ, Lockwood WW, Shah PP, et al. Ubiquitination, localization, and stability of an antiapoptotic BCL2-like protein, BCL2L10/BCLb, are regulated by Ubiquilin1. Proc Natl Acad Sci USA 2012;109:E119-E126.
35. Hippert MM, O'Toole PS, Thorburn A. Autophagy in cancer: good, bad, or both? Cancer Res 2006;66:9349-51.
36. Morselli E, Galluzzi L, Kepp O, et al. Anti- and pro-tumor functions of autophagy. Biochim Biophys Acta 2009;1793:1524-32.
37. Chresta CM, Davies BR, Hickson I, et al. AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res 2010;70:288-98.
38. Chaachouay H, Ohneseit P, Toulany M, et al. Autophagy contributes to resistance of tumor cells to ionizing radiation. Radiother Oncol 2011;99:287-92.
39. Ambros V. The functions of animal microRNAs. Nature 2004;431:350-5.
40. Huang X, Taeb S, Jahangiri S, et al. miRNA-95 mediates radioresistance in tumors by targeting the sphingolipid phosphatase SGPP1. Cancer Res 2013;73:6972-86.
41. Cittelly DM, Dimitrova I, Howe EN, et al. Restoration of miR-200c to ovarian cancer reduces tumor burden and increases sensitivity to paclitaxel. Mol Cancer Ther 2012;11:2556-65.
42. Schickel R, Park SM, Murmann AE, et al. miR-200c regulates induction of apoptosis through CD95 by targeting FAP-1. Mol Cell 2010;38:908-15.
43. Petiot A, Ogier-Denis E, Blommaart EF, et al. Distinct classes of phosphatidylinositol 30-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000;275:992-8.
44. Abedin MJ, Wang D, McDonnell MA, et al. Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 2007;14:500-10.
45. Chen YS, Song HX, Lu Y, et al. Autophagy inhibition contributes to radiation sensitization of esophageal squamous carcinoma cells. Dis Esophagus 2011;24:437-43.
46. Cui J, Cheng Y, Zhang P, et al. Down regulation of miR200c promotes radiation-induced thymic lymphoma by targeting BMI1. J Cell Biochem 2014;115:1033-42.
47. Tang H, Deng M, Tang Y, et al. miR-200b and miR-200c as prognostic factors and mediators of gastric cancer cell progression. Clin Cancer Res 2013;19:5602-12.