MIR-25 modulates invasivenessand dissemination of human prostate cancer cells via regulation of αv-and α6-integrin expression

Cancer Research

Volumn 75, Issue 11, 2015, Pages 2326-2336

  Zoni, E ^a   Van Der Horst, G ^a   Van De Merbel, A F ^a   Chen, L ^b   Rane, J K ^c   Pelger, R C M ^a   Collins, A T ^c   Visakorpi, T ^d   Snaar Jagalska, B E ^b   Maitland, N J ^c   Van Der Pluijm, G ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF YORK   (United Kingdom)

^d TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; CD51 ANTIGEN; MICRORNA; MICRORNA 25; UNCLASSIFIED DRUG; MIRN25 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL SUBPOPULATION; CYTOSKELETON; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; METASTASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROSTATE EPITHELIUM CELL; PROTEIN RNA BINDING; TUMOR INVASION; BIOSYNTHESIS; CARCINOGENESIS; CELL MOTION; CELL PROLIFERATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; MALE; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

CARCINOGENESIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHA6; INTEGRIN ALPHAV; MALE; MICRORNAS; NEOPLASTIC STEM CELLS; PROSTATIC NEOPLASMS;

EID: 84936888406     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2155     Document Type: Article

References (50)

1. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010;19:1893-907.
2. Shackleton M, Quintana E, Fearon ER, Morrison SJ. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009;138: 822-9.
3. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005;5:275-84.
4. Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol 2008;26:2862-70.
5. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005;65:10946-51.
6. Reya T,Morrison SJ, Clarke MF,Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
7. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-66.
8. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-33.
9. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 2008;105:10513-8.
10. Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, et al. Changes in circulatingmicroRNAlevels associated with prostate cancer. Br J Cancer 2012;106:768-74.
11. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM, Guzman-Ramirez N, et al. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 2010;70:5163-73.
12. Rane JK, Scaravilli M, Ylipaa A, PellacaniD,Mann VM, SimmsMS, et al. MicroRNA expression profile of primary prostate cancer stem cells as a source of biomarkers and therapeutic targets. Eur Urol 2015;67: 7-10.
13. Collins AT, Habib FK, Maitland NJ, Neal DE. Identification and isolation of human prostate epithelial stem cells based on alpha(2)beta(1)-integrin expression. J Cell Sci 2001;114:3865-72.
14. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 2004;117:3539-45.
15. Wang X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 2008;14:1012-7.
16. Paraskevopoulou MD, Georgakilas G, Kostoulas N, Vlachos IS, Vergoulis T, Reczko M, et al. DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows. Nucleic Acids Res 2013;41:W169-73.
17. Huang daW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
18. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009;37:1-13.
19. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000;28:27-30.
20. Stoletov K, Montel V, Lester RD, Gonias SL, Klemke R. High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc Natl Acad Sci U S A 2007;104:17406-11.
21. Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 2002;248:307-18.
22. HaldiM, Ton C, Seng WL,McGrath P.Human melanomacells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. Angiogenesis 2006;9:139-51.
23. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is amarker of normal and malignant humanmammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1: 555-67.
24. Douville J, Beaulieu R, Balicki D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cells Dev 2009;18:17-25.
25. Kroon P, Berry PA, Stower MJ, Rodrigues G, Mann VM, Simms M, et al. JAKSTAT blockade inhibits tumor initiation and clonogenic recovery of prostate cancer stem-like cells. Cancer Res 2013;73:5288-98.
26. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20.
27. Kuhn AR, Schlauch K, Lao R, Halayko AJ, Gerthoffer WT, Singer CA. MicroRNA expression in human airway smooth muscle cells: role of miR-25 in regulation of airway smooth muscle phenotype. Am J Respir Cell Mol Biol 2010;42:506-13.
28. Gadea G, Sanz-Moreno V, Self A, Godi A, Marshall CJ. DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr Biol 2008;18:1456-65.
29. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002;110:673-87.
30. Legate KR, Wickstrom SA, Fassler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 2009;23:397-418.
31. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Pelger RC, van der Pluijm G. Integrin alphav expression is required for the acquisition of a metastatic stem/progenitor cell phenotype in human prostate cancer. AmJ Pathol 2011;179:2559-68.
32. Huveneers S, Danen EH. Adhesion signaling-crosstalk between integrins, Src and Rho. J Cell Sci 2009;122:1059-69.
33. Drabsch Y, He S, Zhang L, Snaar-Jagalska BE, Ten Dijke P. Transforming growth factor-beta signalling controls human breast cancer metastasis in a zebrafish xenograft model. Breast Cancer Res 2013;15:R106.
34. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development 2003;130:5281-90.
35. StoletovK, Kato H, Zardouzian E, Kelber J, Yang J, Shattil S, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci 2010;123: 2332-41.
36. Hudson RS, Yi M, Esposito D, Glynn SA, Starks AM, Yang Y, et al. Micro-RNA-106b-25 cluster expression is associated with early disease recurrence and targets caspase-7 and focal adhesion in human prostate cancer. Oncogene 2013;32:4139-47.
37. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, et al. Identification of themiR-106b-25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010;3:ra29.
38. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, et al. Genomic profiling ofmicroRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 2008;68:6162-70.
39. Szczyrba J, Loprich E, Wach S, Jung V, Unteregger G, Barth S, et al. The microRNAprofile of prostate carcinoma obtained by deep sequencing. Mol Cancer Res 2010;8:529-38.
40. Martens-Uzunova ES, Jalava SE, Dits NF, van Leenders GJ, Moller S, Trapman J, et al. Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer. Oncogene 2012;31: 978-91.
41. Polson ES, Lewis JL, Celik H, Mann VM, Stower MJ, Simms MS, et al. Monoallelic expression of TMPRSS2/ERG in prostate cancer stem cells. Nat Commun 2013;4:1623.
42. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNAexpression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-61.
43. LiangH, Studach L, Hullinger RL, Xie J, AndrisaniOM. Down-regulation of RE-1 silencing transcription factor (REST) in advanced prostate cancer by hypoxia-induced miR-106b-25. Exp Cell Res 2014;320:188-99.
44. Brett JO, Renault VM, Rafalski VA, Webb AE, Brunet A. The microRNA cluster miR-106b-25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging 2011;3:108-24.
45. Birnie R, Bryce SD, Roome C, Dussupt V, Droop A, Lang SH, et al. Gene expression profiling of human prostate cancer stem cells reveals a proinflammatory phenotype and the importance of extracellular matrix interactions. Genome Biol 2008;9:R83.
46. Eaton CL, Colombel M, van der Pluijm G, Cecchini M, Wetterwald A, Lippitt J, et al. Evaluation of the frequency of putative prostate cancer stem cells in primary and metastatic prostate cancer. Prostate 2010;70:875-82.
47. Tantivejkul K, Kalikin LM, Pienta KJ. Dynamic process of prostate cancer metastasis to bone. J Cell Biochem 2004;91:706-17.
48. Ricci E, Mattei E, Dumontet C, Eaton CL, Hamdy F, van der Pluije G, et al. Increased expression of putative cancer stem cell markers in the bone marrow of prostate cancer patients is associated with bone metastasis progression. Prostate 2013;73:1738-46.
49. Cluzel C, Saltel F, Lussi J, Paulhe F, Imhof BA, Wehrle-Haller B. The mechanisms and dynamics of (alpha)v(beta)3 integrin clustering in living cells. J Cell Biol 2005;171:383-92.
50. Xu X, Chen Z, Zhao X, Wang J, Ding D, Wang Z, et al. MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma. Biochem Biophys Res Commun 2012;421:640-5.