Regulation of E3 ubiquitin ligase-1 (WWP1) by microRNA-452 inhibits cancer cell migration and invasion in prostate cancer

British Journal of Cancer

Volumn 114, Issue 10, 2016, Pages 1135-1144

  Goto, Yusuke ^a   Kojima, Satoko ^b   Kurozumi, Akira ^a   Kato, Mayuko ^a   Okato, Atsushi ^a   Matsushita, Ryosuke ^c   Ichikawa, Tomohiko ^a   Seki, Naohiko ^a  

^a CHIBA UNIVERSITY   (Japan)

^b TEIKYO UNIVERSITY CHIBA MEDICAL CENTER   (Japan)

^c KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

microRNA; microRNA 452; prostate cancer; tumour suppressor; WW domain containing E3 ubiquitin protein ligase 1

Indexed keywords

MICRORNA; MICRORNA 452; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; MIRN452 MICRORNA, HUMAN; UBIQUITIN PROTEIN LIGASE; WWP1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; MALE; PRIORITY JOURNAL; PROSTATE CANCER; SURVIVAL; TUMOR INVASION; CELL MOTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCEDURES; PROGNOSIS; PROSTATE TUMOR; SURVIVAL ANALYSIS; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICRORNAS; NEOPLASM INVASIVENESS; PROGNOSIS; PROSTATIC NEOPLASMS; SURVIVAL ANALYSIS; UBIQUITIN-PROTEIN LIGASES;

EID: 84963492732     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2016.95     Document Type: Article

References (51)

1. Attard G, Parker C, Eeles RA, Schroder F, Tomlins SA, Tannock I, Drake CG, de Bono JS. (2016). Prostate cancer. Lancet. 387: 70-82.
2. Bartel DP. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 116: 281-297.
3. Bartel DP. (2009). MicroRNAs: target recognition, and regulatory functions. Cell. 136: 215-233.
4. Byrne JA, Chen Y, Martin La Rotta N, Peters GB. (2012). Challenges in identifying candidate amplification targets in human cancers: chromosome 8q21 as a case study. Genes Cancer. 3: 87-101.
5. Chen C, Matesic LE. (2007). The Nedd4-like family of E3 ubiquitin ligases, and cancer. Cancer Metastasis Rev. 26: 587-604.
6. Chen C, Sun X, Guo P, Dong XY, Sethi P, Zhou W, Zhou Z, Petros J, Frierson Jr HF, Vessella RL, Atfi A, Dong JT. (2007). Ubiquitin E3 ligase WWP1 as an oncogenic factor in human prostate cancer. Oncogene. 26: 2386-2394.
7. Chen C, Zhou Z, Liu R, Li Y, Azmi PB, Seth AK. (2008). The WW domain containing E3 ubiquitin protein ligase 1 upregulates ErbB2, and EGFR through RING finger protein 11. Oncogene. 27: 6845-6855.
8. Cheng Q, Cao X, Yuan F, Li G, Tong T. (2014). Knockdown of WWP1 inhibits growth, and induces apoptosis in hepatoma carcinoma cells through the activation of caspase3, and p53. Biochem Biophys Res Commun. 448: 248-254.
9. Crawford ED, Higano CS, Shore ND, Hussain M, Petrylak DP. (2015). Treating patients with metastatic castration resistant prostate cancer: a comprehensive review of available therapies. J Urol. 194: 1537-1547.
10. Elgamal OA, Park JK, Gusev Y, Azevedo-Pouly AC, Jiang J, Roopra A, Schmittgen TD. (2013). Tumor suppressive function of mir-205 in breast cancer is linked to HMGB3 regulation. PLoS One 8: e76402.
11. Friedman RC, Farh KK, Burge CB, Bartel DP. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19: 92-105.
12. Fuse M, Kojima S, Enokida H, Chiyomaru T, Yoshino H, Nohata N, Kinoshita T, Sakamoto S, Naya Y, Nakagawa M, Ichikawa T, Seki N. (2012). Tumor suppressive microRNAs (miR-222, and miR-31) regulate molecular pathways based on microRNA expression signature in prostate cancer. J Hum Genet. 57: 691-699.
13. Garzon R, Calin GA, Croce CM. (2009). MicroRNAs in Cancer. Annu Rev Med. 60: 167-179.
14. Geissler KJ, Jung MJ, Riecken LB, Sperka T, Cui Y, Schacke S, Merkel U, Markwart R, Rubio I, Than ME, Breithaupt C, Peuker S, Seifert R, Kaupp UB, Herrlich P, Morrison H. (2013). Regulation of Son of sevenless by the membrane-Actin linker protein ezrin. Proc Natl Acad Sci USA. 110: 20587-20592.
15. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. (2012). Targeting MET in cancer: rationale, and progress. Nat Rev Cancer. 12: 89-103.
16. Goni GM, Epifano C, Boskovic J, Camacho-Artacho M, Zhou J, Bronowska A, Martin MT, Eck MJ, Kremer L, Grater F, Gervasio FL, Perez-Moreno M, Lietha D. (2014). Phosphatidylinositol 4, 5-bisphosphate triggers activation of focal adhesion kinase by inducing clustering, and conformational changes. Proc Natl Acad Sci USA. 111: E3177-E3186.
17. Goto Y, Kojima S, Nishikawa R, Enokida H, Chiyomaru T, Kinoshita T, Nakagawa M, Naya Y, Ichikawa T, Seki N. (2014). The microRNA-23b/.27b/24-1 cluster is a disease progression marker, and tumor suppressor in prostate cancer. Oncotarget. 5: 7748-7759.
18. Goto Y, Kojima S, Nishikawa R, Kurozumi A, Kato M, Enokida H, Matsushita R, Yamazaki K, Ishida Y, Nakagawa M, Naya Y, Ichikawa T, Seki N. (2015). MicroRNA expression signature of castration-resistant prostate cancer: the microRNA-221/222 cluster functions as a tumour suppressor, and disease progression marker. Br J Cancer. 113: 1055-1065.
19. Goto Y, Kurozumi A, Enokida H, Ichikawa T, Seki N. (2015). Functional significance of aberrantly expressed microRNAs in prostate cancer. Int J Urol. 22: 242-252.
20. Goto Y, Nishikawa R, Kojima S, Chiyomaru T, Enokida H, Inoguchi S, Kinoshita T, Fuse M, Sakamoto S, Nakagawa M, Naya Y, Ichikawa T, Seki N. (2014). Tumour-suppressive microRNA-224 inhibits cancer cell migration, and invasion via targeting oncogenic TPD52 in prostate cancer. FEBS Lett. 588: 1973-1982.
21. Heidenreich A, Bastian PJ, Bellmunt J, Bolla M, Joniau S, van der Kwast T, Mason M, Matveev V, Wiegel T, Zattoni F, Mottet N. (2014). EAU guidelines on prostate cancer. part 1: screening, diagnosis, and local treatment with curative intent-update 2013. Eur Urol. 65: 124-137.
22. Heidenreich A, Bastian PJ, Bellmunt J, Bolla M, Joniau S, van der Kwast T, Mason M, Matveev V, Wiegel T, Zattoni F, Mottet N. (2014). EAU Guidelines on Prostate Cancer. Part II: treatment of advanced, relapsing, and castration-resistant prostate cancer. Eur Urol. 65: 467-479.
23. Iorio MV, Croce CM. (2012). MicroRNA dysregulation in cancer: diagnostics, monitoring, and therapeutics A comprehensive review. EMBO Mol Med. 4: 143-159.
24. Karamouzis MV, Konstantinopoulos PA, Papavassiliou AG. (2009). Targeting MET as a strategy to overcome crosstalk-related resistance to EGFR inhibitors. Lancet Oncol. 10: 709-717.
25. Kelly P, Stemmle LN, Madden JF, Fields TA, Daaka Y, Casey PJ. (2006) A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion. J Biol Chem. 281: 26483-26490.
26. Knoll S, Furst K, Kowtharapu B, Schmitz U, Marquardt S, Wolkenhauer O, Martin H, Putzer BM. (2014). E2F1 induces miR-224/452 expression to drive EMT through TXNIP downregulation. EMBO Rep. 15: 1315-1329.
27. Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nohata N, Fuse M, Ichikawa T, Naya Y, Nakagawa M, Seki N. (2012). Tumour suppressors miR-1, and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer. 106: 405-413.
28. Kojima S, Enokida H, Yoshino H, Itesako T, Chiyomaru T, Kinoshita T, Fuse M, Nishikawa R, Goto Y, Naya Y, Nakagawa M, Seki N. (2014). The tumorsuppressive microRNA-143/145 cluster inhibits cell migration, and invasion by targeting GOLM1 in prostate cancer. J Hum Genet. 59: 78-87.
29. Komuro A, Imamura T, Saitoh M, Yoshida Y, Yamori T, Miyazono K, Miyazawa K. (2004). Negative regulation of transforming growth factor-beta (TGF-beta) signaling by WW domain-containing protein 1 (WWP1). Oncogene. 23: 6914-6923.
30. Kristensen H, Haldrup C, Strand S, Mundbjerg K, Mortensen MM, Thorsen K, Ostenfeld MS, Wild PJ, Arsov C, Goering W, Visakorpi T, Egevad L, Lindberg J, Gronberg H, Hoyer S, Borre M, Orntoft TF, Sorensen KD. (2014). Hypermethylation of the GABREBmiR-452BmiR-224 promoter in prostate cancer predicts biochemical recurrence after radical prostatectomy. Clin Cancer Res. 20: 2169-2181.
31. Kurozumi A, Goto Y, Matsushita R, Fukumoto I, Kato M, Nishikawa R, Sakamoto S, Enokida H, Nakagawa M, Ichikawa T, Seki N. (2016). Tumorsuppressive microRNA-223 inhibits cancer cell migration, and invasion by targeting ITGA3/ITGB1 signaling in prostate cancer. Cancer Sci. 107: 84-94.
32. Laine A, Ronai Z. (2007). Regulation of p53 localization, and transcription by the HECT domain E3 ligase WWP1. Oncogene. 26: 1477-1483.
33. Lewis BP, Burge CB, Bartel DP. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 120: 15-20.
34. Li J, Wei K, Yu H, Jin D, Wang G, Yu B. (2015). Prognostic value of ezrin in various cancers: a systematic review, and updated meta-Analysis. Sci Rep. 5: 17903.
35. Li M, Cai Y, Zhao H, Xu Z, Sun Q, Luo M, Gu L, Meng M, Han X, Sun H. (2015). Overexpression of HMGB3 protein promotes cell proliferation, migration, and is associated with poor prognosis in urinary bladder cancer patients. Tumour Biol. 36: 4785-4792.
36. Li Y, Zhou Z, Chen C. (2008). WW domain-containing E3 ubiquitin protein ligase 1 targets p63 transcription factor for ubiquitin-mediated proteasomal degradation, and regulates apoptosis. Cell Death Differ. 15: 1941-1951.
37. Liu L, Chen K, Wu J, Shi L, Hu B, Cheng S, Li M, Song L. (2013). Downregulation of miR-452 promotes stem-like traits, and tumorigenicity of gliomas. Clin Cancer Res. 19: 3429-3438.
38. Mendell JT. (2008). miRiad roles for the miR-17-92 cluster in development, and disease. Cell. 133: 217-222.
39. Moren A, Imamura T, Miyazono K, Heldin CH, Moustakas A. (2005). Degradation of the tumor suppressor Smad4 by WW, and HECT domain ubiquitin ligases. J Biol Chem. 280: 22115-22123.
40. Nishikawa R, Goto Y, Kurozumi A, Matsushita R, Enokida H, Kojima S, Naya Y, Nakagawa M, Ichikawa T, Seki N. (2015). MicroRNA-205 inhibits cancer cell migration, and invasion via modulation of centromere protein F regulating pathways in prostate cancer. Int J Urol. 22: 867-877.
41. Oneyama C, Yoshikawa Y, Ninomiya Y, Iino T, Tsukita S, Okada M. (2015). Fer tyrosine kinase oligomer mediates, and amplifies Src-induced tumor progression. Oncogene. 35: 501-512.
42. Rasheed SA, Teo CR, Beillard EJ, Voorhoeve PM, Casey PJ. (2013). MicroRNA-182, and microRNA-200a control G-protein subunit alpha-13 (GNA13) expression, and cell invasion synergistically in prostate cancer cells. J Biol Chem. 288: 7986-7995.
43. Ren L, Mendoza A, Zhu J, Briggs JW, Halsey C, Hong ES, Burkett SS, Morrow J, Lizardo MM, Osborne T, Li SQ, Luu HH, Meltzer P, Khanna C. (2015). Characterization of the metastatic phenotype of a panel of established osteosarcoma cells. Oncotarget. 6: 29469-29481.
44. Rubin MA, Varambally S, Beroukhim R, Tomlins SA, Rhodes DR, Paris PL, Hofer MD, Storz-Schweizer M, Kuefer R, Fletcher JA, Hsi BL, Byrne JA, Pienta KJ, Collins C, Sellers WR, Chinnaiyan AM. (2004). Overexpression, amplification, and androgen regulation of TPD52 in prostate cancer. Cancer Res. 64: 3814-3822.
45. Siegel RL, Miller KD, Jemal A. (2015). Cancer statistics, 2015. CA Cancer J Clin. 65: 5-29.
46. Singh R, Kapur N, Mir H, Singh N, Lillard Jr JW, Singh S. (2016). CXCR6-CXCL16 axis promotes prostate cancer by mediating cytoskeleton rearrangement via Ezrin activation, and alphavbeta3 integrin clustering. Oncotarget. 7: 7343-7353.
47. Wang Z, Wang J, Li X, Xing L, Ding Y, Shi P, Zhang Y, Guo S, Shu X, Shan B. (2014). Bortezomib prevents oncogenesis, and bone metastasis of prostate cancer by inhibiting WWP1, Smurf1, and Smurf2. Int J Oncol. 45: 1469-1478.
48. Zheng Q, Sheng Q, Jiang C, Shu J, Chen J, Nie Z, Lv Z, Zhang Y. (2014). MicroRNA-452 promotes tumorigenesis in hepatocellular carcinoma by targeting cyclin-dependent kinase inhibitor 1B. Mol Cell Biochem. 389: 187-195.
49. Zhi X, Chen C. (2012). WWP1: a versatile ubiquitin E3 ligase in signaling, and diseases. Cell Mol Life Sci. 69: 1425-1434.
50. Zhou Z, Liu R, Chen C. (2012). The WWP1 ubiquitin E3 ligase increases TRAIL resistance in breast cancer. Int J Cancer. 130: 1504-1510.
51. Zou X, Levy-Cohen G, Blank M. (2015). Molecular functions of NEDD4 E3 ubiquitin ligases in cancer. Biochim Biophys Acta. 1856: 91-106.