LEF1 targeting EMT in prostate cancer invasion is regulated by miR-34a

Molecular Cancer Research

Volumn 13, Issue 4, 2015, Pages 681-688

  Liang, Jiaqian ^a,b   Li, Yirong ^a   Daniels, Garrett ^a   Sfanos, Karen ^c   De Marzo, Angelo ^c   Wei, Jianjun ^d   Li, Xin ^a,e   Chen, Wenqiang ^f   Wang, Jinhua ^a   Zhong, Xuelin ^a   Melamed, Jonathan ^a   Zhao, Jun ^g   Lee, Peng ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^f GUANGXI MEDICAL UNIVERSITY   (China)

^g HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOID ENHANCER FACTOR 1; MICRORNA 34A; 3' UNTRANSLATED REGION; LEF1 PROTEIN, HUMAN; MICRORNA; MIRN34 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; TUMOR INVASION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOID ENHANCER-BINDING FACTOR 1; MALE; MICRORNAS; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS;

EID: 84928040874     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0503     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Loberg RD, Logothetis CJ, Keller ET, Pienta KJ. Pathogenesis and treatment of prostate cancer bone metastases: targeting the lethal phenotype. J Clin Oncol 2005;23:8232-41.
3. Pienta KJ, Smith DC. Advances in prostate cancer chemotherapy: a new era begins. CA Cancer J Clin 2005;55:300-18; quiz 23-5.
4. Rodriguez-Ubreva J, Ciudad L, van Oevelen C, Parra M, Graf T, Ballestar E. C/EBPa-mediated activation of MicroRNAs 34a and 223 inhibits lef1 expression to achieve efficient reprogramming into macrophages. Mol Cell Biol 2014;34:1145-57.
5. Brabletz T. To differentiate or not-routes towards metastasis. Nat Rev Cancer 2012;12:425-36.
6. Sato M, Shames DS, Hasegawa Y. Emerging evidence of epithelial-tomesenchymal transition in lung carcinogenesis. Respirology 2012;17: 1048-59.
7. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, et al. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010;101:293-9.
8. Ezponda T, Popovic R, Shah MY, Martinez-Garcia E, Zheng Y, Min DJ, et al. The histone methyltransferase MMSET/WHSC1 activates TWIST1 to promote an epithelial-mesenchymal transition and invasive properties of prostate cancer. Oncogene 2013;32:2882-90.
9. Shiota M, Zardan A, Takeuchi A, Kumano M, Beraldi E, Naito S, et al. Clusterin mediates TGF-beta-induced epithelial-mesenchymal transition and metastasis via Twist1 in prostate cancer cells. Cancer Res 2012; 72:5261-72.
10. Zhang S, Wang X, Iqbal S, Wang Y, Osunkoya AO, Chen Z, et al. Epidermal growth factor promotes protein degradation of epithelial protein lost in neoplasm (EPLIN), a putative metastasis suppressor, during epithelial-mesenchymal transition. J Biol Chem 2013;288:1469-79.
11. Cho KH, Choi MJ, Jeong KJ, Kim JJ, Hwang MH, Shin SC, et al. A ROS/ STAT3/HIF-1alpha signaling cascade mediates EGF-induced TWIST1 expression and prostate cancer cell invasion. Prostate 2014;74:528-36.
12. Heuberger J, Birchmeier W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2010;2: a002915.
13. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, et al. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 1999;96:5522-7.
14. Jung HC, Kim K. Identification of MYCBP as a beta-catenin/LEF-1 target using DNA microarray analysis. Life Sci 2005;77:1249-62.
15. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T. beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 1999;155:1033-8.
16. Li Y, Wang L, Zhang M, Melamed J, Liu X, Reiter R, et al. LEF1 in androgenindependent prostate cancer: regulation of androgen receptor expression, prostate cancer growth, and invasion. Cancer Res 2009;69:3332-8.
17. Wu X, Daniels G, Shapiro E, Xu K, Huang H, Li Y, et al. LEF1 identifies androgen-independent epithelium in the developing prostate. Mol Endocrinol 2011;25:1018-26.
18. Wu L, Zhao JC, Kim J, Jin HJ, Wang CY, Yu J. ERG is a critical regulator of Wnt/LEF1 signaling in prostate cancer. Cancer Res 2013;73:6068-79.
19. Zhang K, Waxman DJ. PC3 prostate tumor-initiating cells with molecular profile FAM65Bhigh/MFI2low/LEF1low increase tumor angiogenesis. Mol Cancer 2010;9:319.
20. Bagga S, Pasquinelli AE. Identification and analysis of microRNAs. Genet Eng 2006;27:1-20.
21. Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 2004;5: 396-400.
22. He X, He L, Hannon GJ. The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 2007;67:11099-101.
23. Hermeking H. p53 enters the microRNA world. Cancer Cell 2007;12: 414-8.
24. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010;17:193-9.
25. Siemens H, Neumann J, Jackstadt R, Mansmann U, Horst D, Kirchner T, et al. Detection of miR-34a promoter methylation in combination with elevated expression of c-Met and beta-catenin predicts distantmetastasis of colon cancer. Clin Cancer Res 2013;19:710-20.
26. Bu P, Chen KY, Chen JH, Wang L, Walters J, Shin YJ, et al. A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell 2013;12:602-15.
27. Cha YH, Kim NH, Park C, Lee I, Kim HS, Yook JI. MiRNA-34 intrinsically links p53 tumor suppressor and Wnt signaling. Cell Cycle 2012;11: 1273-81.
28. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, Li XY, et al. p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 2011;4:ra71.
29. Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE, et al. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 2011;195:417-33.
30. Cheng CY, Hwang CI, Corney DC, Flesken-Nikitin A, Jiang L, Oner GM, et al. miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep 2014;6:1000-7.
31. 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.
32. Rokhlin OW, Scheinker VS, Taghiyev AF, Bumcrot D, Glover RA, Cohen MB. MicroRNA-34 mediates AR-dependent p53-induced apoptosis in prostate cancer. Cancer Biol Ther 2008;7:1288-96.
33. Kaller M, Liffers ST, Oeljeklaus S, Kuhlmann K, Roh S, Hoffmann R, et al. Genome-wide characterization ofmiR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol Cell Proteomics 2011;10:M111 010462.
34. Gokey NG, Srinivasan R, Lopez-Anido C, Krueger C, Svaren J. Developmental regulation ofmicroRNA expression in Schwann cells. Mol Cell Biol 2012;32:558-68.
35. Li Y, Ligr M, McCarron JP, Daniels G, Zhang D, Zhao X, et al. Natura-alpha targets forkhead box m1 and inhibits androgen-dependent and-independent prostate cancer growth and invasion. Clin Cancer Res 2011;17: 4414-24.
36. DarshanM, Zheng Q, Fedor HL, Wyhs N, Yegnasubramanian S, Lee P, et al. Biobanking of derivatives from radical retropubic and robot-assisted laparoscopic prostatectomy tissues as part of the prostate cancer biorepository network. Prostate 2014;74:61-9.
37. Becker-Santos DD, Guo Y, Ghaffari M, Vickers ED, Lehman M, Altamirano-DimasM, et al. Integrin-linked kinase as a target for ERG-mediated invasive properties in prostate cancer models. Carcinogenesis 2012;33:2558-67.
38. Zirkel A, Lederer M, Stohr N, Pazaitis N, Huttelmaier S. IGF2BP1 promotes mesenchymal cell properties and migration of tumor-derived cells by enhancing the expression of LEF1 and SNAI2 (SLUG). Nucleic Acids Res 2013;41:6618-36.
39. Wang WJ, Yao Y, Jiang LL, Hu TH, Ma JQ, Liao ZJ, et al. Knockdown of lymphoid enhancer factor 1 inhibits colon cancer progression in vitro and in vivo. PLoS ONE 2013;8:e76596.
40. Liu N, Yang J, Guo S, Xu Y, Zhang M. Genome-wide identification and comparative analysis of conserved and novel microRNAs in grafted watermelon by high-throughput sequencing. PLoS ONE 2013;8:e57359.
41. Zhu ML, Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 2010;24:769-77.
42. Wan X, Liu J, Lu JF, Tzelepi V, Yang J, Starbuck MW, et al. Activation of betacatenin signaling in androgen receptor-negative prostate cancer cells. Clin Cancer Res 2012;18:726-36.
43. Dotto GP, Karine L. miR-34a/SIRT6 in squamous differentiation and cancer. Cell Cycle 2014;13:1055-6.
44. Rokavec M, Oner MG, Li H, Jackstadt R, Jiang L, Lodygin D, et al. IL-6R/ STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest 2014;124:1853-67.
45. Duan W, Xu Y, Dong Y, Cao L, Tong J, Zhou X. Ectopic expression of miR-34a enhances radiosensitivity of non-small cell lung cancer cells, partly by suppressing the LyGDI signaling pathway. J Radiat Res 2013;54:611-9.
46. Corcoran C, Rani S, O'Driscoll L. miR-34a is an intracellular and exosomal predictive biomarker for response to docetaxel with clinical relevance to prostate cancer progression. Prostate 2014;74:1320-34.
47. Franchina T, Amodeo V, Bronte G, Savio G, Ricciardi GR, Picciotto M, et al.CirculatingmiR-22, miR-24 andmiR-34a as novel predictive biomarkers to pemetrexed-based chemotherapy in advanced non-small cell lung cancer. J Cell Physiol 2014;229:97-9.
48. Li L, Xie X, Luo J, Liu M, Xi S, Guo J, et al. Targeted expression of miR-34a using the T-VISA system suppresses breast cancer cell growth and invasion. Mol Ther 2012;20:2326-34.
49. Deng X, Cao M, Zhang J, Hu K, Yin Z, Zhou Z, et al. Hyaluronic acidchitosan nanoparticles for co-delivery of MiR-34a and doxorubicin in therapy against triple negative breast cancer. Biomaterials 2014;35: 4333-44.