Downregulation of Foxo3 and TRIM31 by miR-551b in side population promotes cell proliferation, invasion, and drug resistance of ovarian cancer

Medical Oncology

Volumn 33, Issue 11, 2016, Pages

  Wei, Zhentong ^a   Liu, Yan ^a   Wang, Yishu ^b   Zhang, Yandong ^a   Luo, Qinghua ^a   Man, Xiaxia ^a   Wei, Feng ^d   Yu, Xiaowei ^a,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b Basic Medical College   (China)

^c JILIN UNIVERSITY   (China)

^d BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

Cell invasion; Cell proliferation; Drug resistance; miR 551b; Ovarian cancer; Side population of cancer cells

Indexed keywords

CISPLATIN; MICRORNA; MICRORNA 551B; PROTEIN; TRANSCRIPTION FACTOR FKHRL1; TRIPARTITE MOTIF CONTAINING 31 PROTEIN; UNCLASSIFIED DRUG; FOXO3 PROTEIN, HUMAN; MIRN-551 MICRORNA, HUMAN; TRIM31 PROTEIN, HUMAN; TRIPARTITE MOTIF PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL INVASION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; OVARIAN NEOPLASMS; PATHOLOGY; SCID MOUSE; TUMOR CELL CULTURE;

ANIMALS; CISPLATIN; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; FORKHEAD BOX PROTEIN O3; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, SCID; MICRORNAS; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; TRIPARTITE MOTIF PROTEINS; TUMOR CELLS, CULTURED; UBIQUITIN-PROTEIN LIGASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84991494214     PISSN: 13570560     EISSN: 1559131X     Source Type: Journal    
DOI: 10.1007/s12032-016-0842-9     Document Type: Article

References (50)

1. Jelovac D, Armstrong DK. Recent progress in the diagnosis and treatment of ovarian cancer. CA Cancer J Clin. 2011;61(3):183–203.
2. Coleman RL, Monk BJ, Sood AK, Herzog TJ. Latest research and treatment of advanced-stage epithelial ovarian cancer. Nat Rev Clin Oncol. 2013;10(4):211–24.
3. Vaughan S, Coward JI, Bast RC Jr, Berchuck A, Berek JS, Brenton JD, Coukos G, Crum CC, Drapkin R, Etemadmoghadam D, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer. 2011;11(10):719–25.
4. Harrington BS, He Y, Davies CM, Wallace SJ, Adams MN, Beaven EA, Roche DK, Kennedy C, Chetty NP, Crandon AJ, et al. Cell line and patient-derived xenograft models reveal elevated CDCP1 as a target in high-grade serous ovarian cancer. Br J Cancer. 2016;114(4):417–26.
5. Cooke SL, Ng CK, Melnyk N, Garcia MJ, Hardcastle T, Temple J, Langdon S, Huntsman D, Brenton JD. Genomic analysis of genetic heterogeneity and evolution in high-grade serous ovarian carcinoma. Oncogene. 2010;29(35):4905–13.
6. Stronach EA, Alfraidi A, Rama N, Datler C, Studd JB, Agarwal R, Guney TG, Gourley C, Hennessy BT, Mills GB, et al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res. 2011;71(13):4412–22.
7. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature. 2008;452(7187):650–3.
8. O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445(7123):106–10.
9. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756–60.
10. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458(7239):780–3.
11. de The H, Chen Z. Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat Rev Cancer. 2010;10(11):775–83.
12. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi AL. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444(7120):761–5.
13. Shah MM, Landen CN. Ovarian cancer stem cells: are they real and why are they important? Gynecol Oncol. 2014;132(2):483–9.
14. Flesken-Nikitin A, Hwang CI, Cheng CY, Michurina TV, Enikolopov G, Nikitin AY. Ovarian surface epithelium at the junction area contains a cancer-prone stem cell niche. Nature. 2013;495(7440):241–5.
15. Gilks CB, Irving J, Kobel M, Lee C, Singh N, Wilkinson N, McCluggage WG. Incidental nonuterine high-grade serous carcinomas arise in the fallopian tube in most cases: further evidence for the tubal origin of high-grade serous carcinomas. Am J Surg Pathol. 2015;39(3):357–64.
16. Sherman-Baust CA, Kuhn E, Valle BL, Shih Ie M, Kurman RJ, Wang TL, Amano T, Ko MS, Miyoshi I, Araki Y, et al. A genetically engineered ovarian cancer mouse model based on fallopian tube transformation mimics human high-grade serous carcinoma development. J Pathol. 2014;233(3):228–37.
17. Burgos-Ojeda D, Rueda BR, Buckanovich RJ. Ovarian cancer stem cell markers: prognostic and therapeutic implications. Cancer Lett. 2012;322(1):1–7.
18. Ffrench B, Gasch C, O’Leary JJ, Gallagher MF. Developing ovarian cancer stem cell models: laying the pipeline from discovery to clinical intervention. Mol Cancer. 2014;13:262.
19. Oates JE, Grey BR, Addla SK, Samuel JD, Hart CA, Ramani VA, Brown MD, Clarke NW. Hoechst 33342 side population identification is a conserved and unified mechanism in urological cancers. Stem Cells Dev. 2009;18(10):1515–22.
20. Rizzo S, Hersey JM, Mellor P, Dai W, Santos-Silva A, Liber D, Luk L, Titley I, Carden CP, Box G, et al. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther. 2011;10(2):325–35.
21. Hu L, McArthur C, Jaffe RB. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br J Cancer. 2010;102(8):1276–83.
22. Wei Z, Lv S, Wang Y, Sun M, Chi G, Guo J, Song P, Fu X, Zhang S, Li Y. Biological characteristics of side population cells in a self-established human ovarian cancer cell line. Oncol Lett. 2016;12(1):41–8.
23. Ling H, Fabbri M, Calin GA. MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov. 2013;12(11):847–65.
24. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.
25. Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med. 2014;20(8):460–9.
26. Yang Y, Li X, Yang Q, Wang X, Zhou Y, Jiang T, Ma Q, Wang YJ. The role of microRNA in human lung squamous cell carcinoma. Cancer Genet Cytogenet. 2010;200(2):127–33.
27. Haldrup C, Kosaka N, Ochiya T, Borre M, Hoyer S, Orntoft TF, Sorensen KD. Profiling of circulating microRNAs for prostate cancer biomarker discovery. Drug Deliv Transl Res. 2014;4(1):19–30.
28. Chaluvally-Raghavan P, Jeong KJ, Pradeep S, Silva AM, Yu S, Liu W, Moss T, Rodriguez-Aguayo C, Zhang D, Ram P, et al. Direct upregulation of STAT3 by microRNA-551b-3p deregulates growth and metastasis of ovarian cancer. Cell Rep. 2016;15(7):1493–504.
29. Lin S, Gregory RI. MicroRNA biogenesis pathways in cancer. Nat Rev Cancer. 2015;15(6):321–33.
30. Zhou JN, Zeng Q, Wang HY, Zhang B, Li ST, Nan X, Cao N, Fu CJ, Yan XL, Jia YL, et al. MicroRNA-125b attenuates epithelial-mesenchymal transitions and targets stem-like liver cancer cells through small mothers against decapentaplegic 2 and 4. Hepatology. 2015;62(3):801–15.
31. Jones MF, Hara T, Francis P, Li XL, Bilke S, Zhu Y, Pineda M, Subramanian M, Bodmer WF, Lal A. The CDX1-microRNA-215 axis regulates colorectal cancer stem cell differentiation. Proc Natl Acad Sci USA. 2015;112(13):E1550–8.
32. Li C, Ding H, Tian J, Wu L, Wang Y, Xing Y, Chen M. Forkhead box protein C2 promotes epithelial-mesenchymal transition, migration and invasion in cisplatin–resistant human ovarian cancer cell line (SKOV3/CDDP). Cell Physiol Biochem. 2016;39(3):1098–110.
33. Zhan Q, Wang C, Ngai S. Ovarian cancer stem cells: a new target for cancer therapy. Biomed Res Int. 2013;2013:916819.
34. Yalcin S, Zhang X, Luciano JP, Mungamuri SK, Marinkovic D, Vercherat C, Sarkar A, Grisotto M, Taneja R, Ghaffari S. Foxo3 is essential for the regulation of ataxia telangiectasia mutated and oxidative stress-mediated homeostasis of hematopoietic stem cells. J Biol Chem. 2008;283(37):25692–705.
35. Li H, Zhang Y, Zhang Y, Bai X, Peng Y, He P. TRIM31 is downregulated in non-small cell lung cancer and serves as a potential tumor suppressor. Tumour Biol. 2014;35(6):5747–52.
36. Watanabe M, Tsukiyama T, Hatakeyama S. TRIM31 interacts with p52(Shc) and inhibits Src-induced anchorage-independent growth. Biochem Biophys Res Commun. 2009;388(2):422–7.
37. Lengyel E. Ovarian cancer development and metastasis. Am J Pathol. 2010;177(3):1053–64.
38. Tan DS, Agarwal R, Kaye SB. Mechanisms of transcoelomic metastasis in ovarian cancer. Lancet Oncol. 2006;7(11):925–34.
39. Boesch M, Zeimet AG, Reimer D, Schmidt S, Gastl G, Parson W, Spoeck F, Hatina J, Wolf D, Sopper S. The side population of ovarian cancer cells defines a heterogeneous compartment exhibiting stem cell characteristics. Oncotarget. 2014;5(16):7027–39.
40. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin DT, Donahoe PK. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci USA. 2006;103(30):11154–9.
41. Beck B, Blanpain C. Unravelling cancer stem cell potential. Nat Rev Cancer. 2013;13(10):727–38.
42. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, Kim JH, Kim JW, Kim S. MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res. 2008;14(9):2690–5.
43. Zhou X, Hu Y, Dai L, Wang Y, Zhou J, Wang W, Di W, Qiu L. MicroRNA-7 inhibits tumor metastasis and reverses epithelial-mesenchymal transition through AKT/ERK1/2 inactivation by targeting EGFR in epithelial ovarian cancer. PLoS One. 2014;9(5):e96718.
44. Tang H, Yao L, Tao X, Yu Y, Chen M, Zhang R, Xu C. miR-9 functions as a tumor suppressor in ovarian serous carcinoma by targeting TLN1. Int J Mol Med. 2013;32(2):381–8.
45. Boac BM, Xiong Y, Marchion DC, Abbasi F, Bush SH, Ramirez IJ, Khulpateea BR, Clair McClung E, Berry AL, Bou Zgheib N, et al. Micro-RNAs associated with the evolution of ovarian cancer cisplatin resistance. Gynecol Oncol. 2016;140(2):259–63.
46. He Y, Wu AC, Harrington BS, Davies CM, Wallace SJ, Adams MN, Palmer JS, Roche DK, Hollier BG, Westbrook TF, et al. Elevated CDCP1 predicts poor patient outcome and mediates ovarian clear cell carcinoma by promoting tumor spheroid formation, cell migration and chemoresistance. Oncogene. 2016;35(4):468–78.
47. Wan YW, Mach CM, Allen GI, Anderson ML, Liu Z. On the reproducibility of TCGA ovarian cancer microRNA profiles. PLoS One. 2014;9(1):e87782.
48. Xu X, Wells A, Padilla MT, Kato K, Kim KC, Lin Y. A signaling pathway consisting of miR-551b, catalase and MUC1 contributes to acquired apoptosis resistance and chemoresistance. Carcinogenesis. 2014;35(11):2457–66.
49. Levanon K, Sapoznik S, Bahar-Shany K, Brand H, Shapira-Frommer R, Korach J, Hirsch MS, Roh MH, Miron A, Liu JF, et al. FOXO3a loss is a frequent early event in high-grade pelvic serous carcinogenesis. Oncogene. 2014;33(35):4424–32.
50. Sugiura T, Miyamoto K. Characterization of TRIM31, upregulated in gastric adenocarcinoma, as a novel RBCC protein. J Cell Biochem. 2008;105(4):1081–91.