MiR-154∗ and miR-379 in the DLK1-DIO3 MicroRNA mega-cluster regulate epithelial to mesenchymal transition and bone metastasis of prostate cancer

Clinical Cancer Research

Volumn 20, Issue 24, 2014, Pages 6559-6569

  Gururajan, Murali ^a   Josson, Sajni ^a   Chu, Gina Chia Yi ^a   Lu, Chia Lun ^a   Lu, Yi Tsung ^a   Haga, Christopher L ^b   Zhau, Haiyen E ^a   Liu, Chunyan ^a   Lichterman, Jake ^a   Duan, Peng ^a   Posadas, Edwin M ^a   Chung, Leland W K ^a  

^a Samuel Oschin Comprehensive Cancer Institute   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEIODINASE IODOTHYRONINE 3; DELTA LIKE 1 HOMOLOG; MICRORNA; MICRORNA 154; MICRORNA 379; TUMOR PROTEIN; UNCLASSIFIED DRUG; DLK1 PROTEIN, HUMAN; IODIDE PEROXIDASE; IODOTHYRONINE DEIODINASE TYPE III; MEMBRANE PROTEIN; MIRN154 MICRORNA, HUMAN; MIRN379 MICRORNA, HUMAN; SIGNAL PEPTIDE;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; CANCER CELL CULTURE; CANCER GROWTH; CANCER SURVIVAL; CELL INVASION; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC MANIPULATION; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; RNA ANALYSIS; SOFT TISSUE METASTASIS; WESTERN BLOTTING; ANIMAL; BONE TUMOR; CANCER GRADING; DISEASE MODEL; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; METASTASIS; MULTIGENE FAMILY; PATHOLOGY; PROSTATE TUMOR; RNA INTERFERENCE; SECONDARY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE REGULATORY NETWORKS; HETEROGRAFTS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; IODIDE PEROXIDASE; MALE; MEMBRANE PROTEINS; MICE; MICRORNAS; MULTIGENE FAMILY; NEOPLASM GRADING; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; RNA INTERFERENCE;

EID: 84919742319     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-1784     Document Type: Article

References (43)

1. Wellner U, Schubert J, Burk UC, Schmalhofer O., Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009;11:1487-95.
2. Liu C, Kelnar K, Liu B., Chen X, Calhoun-Davis T, Li H, et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011;17:211-5.
3. Han Z, He H, Zhang F., Huang Z, Liu Z, Jiang H., et al. Spatiotemporal expression pattern of Mirg, an imprinted non-coding gene, during mouse embryogenesis. J Mol Histol 2012;43:1-8.
4. Lim L, Balakrishnan A, Huskey N., Jones KD, Jodari M, Ng R, et al. MiR-494 within an oncogenic MicroRNA megacluster regulates G1/S transition in liver tumorigenesis through suppression of MCC. Hepatology 2014;59:202-15
5. Luk JM, Burchard J, Zhang C., Liu AM, Wong KF, Shek FH, et al. DLK1-DIO3 genomic imprinted microRNA cluster at 14q32.2 defines a stemlike subtype of hepatocellular carcinoma associated with poor survival. J Biol Chem 2011;286:30706-13.
6. Haga CL, Phinney DG. MicroRNAs in the imprinted DLK1-DIO3 region repress the epithelial-to-mesenchymal transition by targeting the TWIST1 protein signaling network. J Biol Chem 2012;287:42695-707.
7. Lempiainen H, Couttet P, Bolognani F., Muller A, Dubost V, Luisier R., et al. Identification of Dlk1-Dio3 imprinted gene cluster noncoding RNAs as novel candidate biomarkers for liver tumor promotion. Toxicol Sci 2013;131:375-86.
8. Valdmanis PN, Roy-Chaudhuri B, Kim HK, Sayles LC, Zheng Y, Chuang CH, et al. Upregulation of the microRNA cluster at the Dlk1-Dio3 locus in lung adenocarcinoma. Oncogene 2013 Dec 9. [Epub ahead of print].
9. Cazzoli R, Buttitta F, Di Nicola M, Malatesta S, Marchetti A., Rom WN, et al. microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer. J Thorac Oncol 2013;8:1156-62.
10. Li S, Meng H, Zhou F., Zhai L, Zhang L, Gu F., et al. MicroRNA-132 is frequently down-regulated in ductal carcinoma in situ (DCIS) of breast and acts as a tumor suppressor by inhibiting cell proliferation. Pathol Res Pract 2013;209:179-83.
11. Nguyen HC, Xie W, Yang M., Hsieh CL, Drouin S, Lee GS, et al. Expression differences of circulating microRNAs in metastatic castration resistant prostate cancer and low-risk, localized prostate cancer. Prostate 2013;73:346-54.
12. Josson S, Gururajan M, Hu P., Shao C, Chu GC, Zhau HE, et al. miR-409-3p/-5p promotes tumorigenesis, epithelial to mesenchymal transition and bone metastasis of human prostate cancer. Clin Cancer Res 2014;20:4636-46.
13. Xu J, Wang R, Xie ZH, Odero-Marah V, Pathak S, Multani A., et al. Prostate cancer metastasis: role of the host microenvironment in promoting epithelial to mesenchymal transition and increased bone and adrenal gland metastasis. Prostate 2006;66:1664-73.
14. Thalmann GN, Sikes RA, Wu TT, Degeorges A., Chang SM, Ozen M, et al. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate 2000;44:91-103.
15. Josson S, Sung SY, Lao K, Chung LW, Johnstone PA. Radiation modulation of microRNA in prostate cancer cell lines. Prostate 2008;68:1599-606.
16. Taylor BS, Schultz N, Hieronymus H., Gopalan A, Xiao Y, Carver B., et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.
17. Gao J, Aksoy BA, Dogrusoz U, Dresdner G., Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Sig 2013;6:pl1.
18. Nomura T, Huang WC, Zhau HE, Wu D., Xie Z, Mimata H, et al. Beta2-microglobulin promotes the growth of human renal cell carcinoma through the activation of the protein kinase A, cyclic AMP-responsive element-binding protein, and vascular endothelial growth factor axis. Clin Cancer Res 2006;12:7294-305.
19. Hu P, Chu GC, Zhu G, Yang H., Luthringer D, Prins G, et al. Multiplexed quantum dot labeling of activated c-Met signaling in castration-resistant human prostate cancer. PloS ONE 2011;6:e28670.
20. Josson S, Nomura T, Lin JT, Huang WC, Wu D, Zhau HE, et al. beta2-microglobulin induces epithelial to mesenchymal transition and confers cancer lethality and bone metastasis in human cancer cells. Cancer Res 2011;71:2600-10.
21. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, et al. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res 1994;54:2577-81.
22. Liu L, Luo GZ, Yang W, Zhao X., Zheng Q, Lv Z, et al. Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem 2010;285:19483-90.
23. Stadtfeld M, Apostolou E, Akutsu H., Fukuda A, Follett P, Natesan S., et al. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 2010;465:175-81.
24. Huang WC, Wu D, Xie Z, Zhau HE, Nomura T, Zayzafoon M, et al. beta2-microglobulin is a signaling and growth-promoting factor for human prostate cancer bone metastasis. Cancer Res 2006;66:9108-16.
25. Solomon DA, Kim T, Diaz-Martinez LA, Fair J., Elkahloun AG, Harris BT, et al. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science 2011;333:1039-43.
26. Zhau HE, Odero-Marah V, Lue HW, Nomura T., Wang R, Chu G, et al. Epithelial to mesenchymal transition (EMT) in human prostate cancer: lessons learned from ARCaP model. Clin Exp Metastasis 2008;25: 601-10.
27. Odero-Marah VA, Wang R, Chu G., Zayzafoon M, Xu J, Shi C., et al. Receptor activator of NF-kappaB Ligand (RANKL) expression is associated with epithelial to mesenchymal transition in human prostate cancer cells. Cell Res 2008;18:858-70.
28. Formosa A, Markert EK, Lena AM, Italiano D., Finazzi-Agro E, Levine AJ, et al. MicroRNAs, miR-154, miR-299-5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485-3p, miR-495 and miR-654-3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells. Oncogene 2013 Oct 28. [Epub ahead of print].
29. Zhu C, Li J, Cheng G., Zhou H, Tao L, Cai H., et al. miR-154 inhibits EMT by targeting HMGA2 in prostate cancer cells. Mol Cell Biochem 2013;379:69-75.
30. Zhu C, Shao P, Bao M., Li P, Zhou H, Cai H., et al. miR-154 inhibits prostate cancer cell proliferation by targeting CCND2. Urol Oncol 2014;32:31.e9-16.
31. Kim MS, Kim SS, Je EM, Yoo NJ, Lee SH. Mutational and expressional analyses of STAG2 gene in solid cancers. Neoplasma 2012;59:524-9.
32. Edlund S, Bu S, Schuster N., Aspenstrom P, Heuchel R, Heldin NE, et al. Transforming growth factor-beta1 (TGF-beta)-induced apoptosis of prostate cancer cells involves Smad7-dependent activation of p38 by TGF-beta-activated kinase 1 and mitogen-activated protein kinase kinase 3. Mol Biol Cell 2003;14:529-44.
33. Nik AM, Reyahi A, Ponten F., Carlsson P. Foxf2 in intestinal fibroblasts reduces numbers of Lgr5(+) stem cells and adenoma formation by inhibiting Wnt signaling. Gastroenterology 2013;144:1001-11.
34. Gonzalez-Nieves R., Desantis AI, Cutler ML. Rsu1 contributes to regulation of cell adhesion and spreading by PINCH1-dependent and - independent mechanisms. J Cell Commun Signal 2013;7:279-93
35. Dougherty GW, Jose C, Gimona M., Cutler ML. The Rsu-1-PINCH1-ILK complex is regulated by Ras activation in tumor cells. Eur J Cell Biol 2008;87:721-34.
36. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxiainducible factors for oxygen-dependent proteolysis. Nature 1999;399: 271-5.
37. Palayoor ST, Burgos MA, Shoaibi A, Tofilon PJ, Coleman CN. Effect of radiation and ibuprofen on normoxic renal carcinoma cells overex-pressing hypoxia-inducible factors by loss of von Hippel-Lindau tumor suppressor gene function. Clin Cancer Res 2004;10:4158-64.
38. Iwata S, Takenobu H, Kageyama H., Koseki H, Ishii T, Nakazawa A., et al. Polycomb group molecule PHC3 regulates polycomb complex composition and prognosis of osteosarcoma. Cancer Sci 2010; 101:1646-52.
39. Kurata A, Katayama R, Watanabe T., Tsuruo T, Fujita N. TUSC4/NPRL2, a novel PDK1-interacting protein, inhibits PDK1 tyrosine phosphorylation and its downstream signaling. Cancer Sci 2008;99: 1827-34.
40. Bar-Peled L., Chantranupong L, Cherniack AD, Chen WW, Ottina KA, Grabiner BC, et al. A Tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 2013;340:1100-6.
41. Maddika S, Ande SR, Panigrahi S, Paranjothy T., Weglarczyk K, Zuse A, et al. Cell survival, cell death and cell cycle pathways are intercon-nected: implications for cancer therapy. Drug Resist Updat 2007;10: 13-29.
42. Lenferink AE, Cantin C, Nantel A., Wang E, Durocher Y, Banville M., et al. Transcriptome profiling of a TGF-beta-induced epithelial-to-mesenchymal transition reveals extracellular clusterin as a target for therapeutic antibodies. Oncogene 2010;29: 831-44.
43. Bryant RJ, Pawlowski T, Catto JW, Marsden G., Vessella RL, Rhees B, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer 2012;106:768-74.