Glucocorticoids mediate induction of microRNA-708 to suppress ovarian cancer metastasis through targeting Rap1B

Nature Communications

Volumn 6, Issue , 2015, Pages

  Lin, Kai Ti ^a   Yeh, Yu Ming ^a   Chuang, Chi Mu ^b,c   Yang, Scarlett Y ^a   Chang, Jer Wei ^a   Sun, Shu Pin ^a   Wang, Yi Shiang ^a,d   Chao, Kuan Chong ^b   Wang, Lu Hai ^a  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; INTEGRIN; MICRORNA; MICRORNA 146A; MICRORNA 200; MICRORNA 218; MICRORNA 708; RAP PROTEIN; RAS RELATED PROTEIN RAP1B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; LUCIFERASE; MIRN708 MICRORNA, HUMAN; RAP1B PROTEIN, HUMAN;

ADHESION; CANCER; CELLS AND CELL COMPONENTS; CHEMOTHERAPY; HORMONE; INHIBITION; RNA; RODENT; TUMOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLUMINESCENCE; BREAST CANCER; CANCER INHIBITION; CANCER STAGING; CANCER SURVIVAL; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CONTROLLED STUDY; CPG ISLAND; DOWN REGULATION; ENZYME REPRESSION; FOCAL ADHESION; GENE; GENE EXPRESSION; GENE INDUCTION; GENE SEQUENCE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; MOUSE; NONHUMAN; ODZ4 GENE; OVARY METASTASIS; OVERALL SURVIVAL; PANCREAS CARCINOMA; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; RECURRENCE FREE SURVIVAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; TUMOR INVASION; TUMOR VOLUME; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; CELL MOTION; DRUG EFFECTS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; NEOPLASM METASTASIS; OVARY TUMOR; PREVENTION AND CONTROL; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; CHROMATIN IMMUNOPRECIPITATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOCORTICOIDS; HETEROGRAFTS; HUMANS; IN SITU HYBRIDIZATION; LUCIFERASES; MICE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; RAP GTP-BINDING PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84931277611     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6917     Document Type: Article

References (43)

1. Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69-90 (2011).
2. Cannistra, S. A. Cancer of the ovary. N. Engl. J. Med. 351, 2519-2529 (2004).
3. Hennessy, B. T., Coleman, R. L. & Markman, M. Ovarian cancer. Lancet 374, 1371-1382 (2009).
4. Gennari, A., Salvadori, B., Tognoni, A. & Conte, P. F. Rapid intravenous premedication with dexamethasone prevents hypersensitivity reactions to paclitaxel. Ann. Oncol, 7, 978-979 (1996).
5. Runnebaum, I. B. & Bruning, A. Glucocorticoids inhibit cell death in ovarian cancer and up-regulate caspase inhibitor cIAP2. Clin. Cancer Res. 11, 6325-6332 (2005).
6. Zhang, C. et al. Glucocorticoid-mediated inhibition of chemotherapy in ovarian carcinomas. Int. J. Oncol. 28, 551-558 (2006).
7. Sui, M., Chen, F., Chen, Z. & Fan, W. Glucocorticoids interfere with therapeutic efficacy of paclitaxel against human breast and ovarian xenograft tumors. Int. J. Cancer 119, 712-717 (2006).
8. Munstedt, K., Borces, D., Bohlmann, M. K., Zygmunt, M. & von Georgi, R. Glucocorticoid administration in antiemetic therapy: is it safe? Cancer 101, 1696-1702 (2004).
9. Rubenstein, N. M., Guan, Y., Woo, P. L. & Firestone, G. L. Glucocorticoid down-regulation of RhoA is required for the steroid-induced organization of the junctional complex and tight junction formation in rat mammary epithelial tumor cells. J. Biol. Chem. 278, 10353-10360 (2003).
10. Zheng, Y., Izumi, K., Li, Y., Ishiguro, H. & Miyamoto, H. Contrary regulation of bladder cancer cell proliferation and invasion by dexamethasone-mediated glucocorticoid receptor signals. Mol. Cancer Ther. 11, 2621-2632 (2012).
11. Law, M. E. et al. Glucocorticoids and histone deacetylase inhibitors cooperate to block the invasiveness of basal-like breast cancer cells through novel mechanisms. Oncogene 32, 1316-1329 (2013).
12. Saini, S. et al. MicroRNA-708 induces apoptosis and suppresses tumorigenicity in renal cancer cells. Cancer Res. 71, 6208-6219 (2011).
13. Saini, S. et al. miRNA-708 control of CD44(+) prostate cancer-initiating cells. Cancer Res. 72, 3618-3630 (2012).
14. Ryu, S. et al. Suppression of miRNA-708 by polycomb group promotes metastases by calcium-induced cell migration. Cancer Cell 23, 63-76 (2013).
15. Yeh, Y. M., Chuang, C. M., Chao, K. C. & Wang, L. H. MicroRNA-138 suppresses ovarian cancer cell invasion and metastasis by targeting SOX4 and HIF-1alpha. Int. J. Cancer (2013).
16. Hwang, S. J. et al. MicroRNA-146a suppresses metastatic activity in brain metastasis. Mol. Cell 34, 329-334 (2012).
17. Zhang, H. F., Xu, L. Y. & Li, E. M. A family of pleiotropically acting microRNAs in cancer progression, miR-200: potential cancer therapeutic targets. Curr. Pharm. Design 20, 1896-1903 (2013).
18. Wu, D. W., Cheng, Y. W., Wang, J., Chen, C. Y. & Lee, H. Paxillin predicts survival and relapse in non-small cell lung cancer by microRNA-218 targeting. Cancer Res. 70, 10392-10401 (2010).
19. Han, B. W. et al. A set of miRNAs that involve in the pathways of drug resistance and leukemic stem-cell differentiation is associated with the risk of relapse and glucocorticoid response in childhood ALL. Hum. Mol. Genet. 20, 4903-4915 (2011).
20. Behrman, S., Acosta-Alvear, D. & Walter, P. A CHOP-regulated microRNA controls rhodopsin expression. J. Cell Biol. 192, 919-927 (2011).
21. Kinbara, K., Goldfinger, L. E., Hansen, M., Chou, F. L. & Ginsberg, M. H. Ras GTPases: integrins' friends or foes? Nature reviews. Mol. Cell Biol. 4, 767-776 (2003).
22. Boettner, B. & Van Aelst, L. Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 21, 684-693 (2009).
23. Bos, J. L. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17, 123-128 (2005).
24. Robin, T. P. et al. EWS/FLI1 regulates EYA3 in Ewing sarcoma via modulation of miRNA-708, resulting in increased cell survival and chemoresistance. Mol. Cancer Res. 10, 1098-1108 (2012).
25. Bokoch, G. M. Biology of the Rap proteins, members of the ras superfamily of GTP-binding proteins. Biochem. J. 289, 17-24 (1993).
26. Huang, M. et al. EGFR-dependent pancreatic carcinoma cell metastasis through Rap1 activation. Oncogene 31, 2783-2793 (2012).
27. Bischoff, A. et al. miR-149 functions as a tumor suppressor by controlling breast epithelial cell migration and invasion. Cancer Res. 74, 5256-5265 (2014).
28. Benlimame, N. et al. FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J. Cell Biol. 171, 505-516 (2005).
29. Nakamura, K., Yano, H., Schaefer, E. & Sabe, H. Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration: analysis of specific phosphorylation events using site-directed antibodies. Oncogene 20, 2626-2635 (2001).
30. Duchniewicz, M. et al. Rap1A-deficient T and B cells show impaired integrin-mediated cell adhesion. Mol. Cell Biol. 26, 643-653 (2006).
31. Chrzanowska-Wodnicka, M., Kraus, A. E., Gale, D., White, 2nd G. C. &Vansluys, J. Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood 111, 2647-2656 (2008).
32. Wittchen, E. S., Aghajanian, A. & Burridge, K. Isoform-specific differences between Rap1A and Rap1B GTPases in the formation of endothelial cell junctions. Small GTPases 2, 65-76 (2011).
33. Schwamborn, J. C. & Puschel, A. W. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7, 923-929 (2004).
34. Lyle, K. S., Raaijmakers, J. H., Bruinsma, W. & Bos, J. L. & de Rooij, J. cAMP-induced Epac-Rap activation inhibits epithelial cell migration by modulating focal adhesion and leading edge dynamics. Cell. Signal. 20, 1104-1116 (2008).
35. Freeman, S. A. et al. Preventing the activation or cycling of the Rap1 GTPase alters adhesion and cytoskeletal dynamics and blocks metastatic melanoma cell extravasation into the lungs. Cancer Res. 70, 4590-4601 (2010).
36. Gao, L. et al. Ras-associated protein-1 regulates extracellular signal-regulated kinase activation and migration in melanoma cells: two processes important to melanoma tumorigenesis and metastasis. Cancer Res. 66, 7880-7888 (2006).
37. Magliozzi, R. et al. Control of epithelial cell migration and invasion by the IKKbeta- and CK1alpha-mediated degradation of RAPGEF2. Dev. Cell 27, 574-585 (2013).
38. Hernandez-Varas, P. et al. Rap1-GTP-interacting adaptor molecule (RIAM) protein controls invasion and growth of melanoma cells. J. Biol. Chem. 286, 18492-18504 (2011).
39. Kim, W. J., Gersey, Z. & Daaka, Y. Rap1GAP regulates renal cell carcinoma invasion. Cancer Lett. 320, 65-71 (2012).
40. Yajnik, V. et al. DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell 112, 673-684 (2003).
41. Zhang, M. et al. miR-518b is down-regulated, and involved in cell proliferation and invasion by targeting Rap1b in esophageal squamous cell carcinoma. FEBS Lett. 586, 3508-3521 (2012).
42. Sachdev, P., Zeng, L. & Wang, L. H. Distinct role of phosphatidylinositol 3-kinase and Rho family GTPases in Vav3-induced cell transformation, cell motility, and morphological changes. J. Biol. Chem. 277, 17638-17648 (2002).
43. Ross, S. H. et al. Ezrin is required for efficient Rap1-induced cell spreading. J. Cell Sci. 124, 1808-1818 (2011).