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Non-coding RNAs in Prostate Cancer: From Discovery to Clinical Applications

  • Yvonne CederEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 886)

Abstract

Prostate cancer is a heterogeneous disease for which the molecular mechanisms are still not fully elucidated. Prostate cancer research has traditionally focused on genomic and epigenetic alterations affecting the proteome, but over the last decade non-coding RNAs, especially microRNAs, have been recognized to play a key role in prostate cancer progression. A considerable number of individual microRNAs have been found to be deregulated in prostate cancer and their biological significance elucidated in functional studies. This review will delineate the current advances regarding the involvement of microRNAs and their targets in prostate cancer biology as well as their potential usage in the clinical management of the disease. The main focus will be on microRNAs contributing to initiation and progression of prostate cancer, including androgen signalling, cellular plasticity, stem cells biology and metastatic processes. To conclude, implications on potential future microRNA-based therapeutics based on the recent advances regarding the interplay between microRNAs and their targets are discussed.

Keywords

MicroRNAs Prostatic neoplasms Androgen receptor Epithelial-mesenchymal transition Neoplasm metastasis 

References

  1. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM (2008) Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68:6162–6170PubMedPubMedCentralCrossRefGoogle Scholar
  2. Amir S, Ma AH, Shi XB, Xue L, Kung HJ, Devere White RW (2013) Oncomir miR-125b suppresses p14(ARF) to modulate p53-dependent and p53-independent apoptosis in prostate cancer. PLoS One 8:e61064PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arora R, Koch MO, Eble JN, Ulbright TM, Li L, Cheng L (2004) Heterogeneity of Gleason grade in multifocal adenocarcinoma of the prostate. Cancer 100:2362–2366PubMedCrossRefGoogle Scholar
  4. Bao B, Ahmad A, Kong D, Ali S, Azmi AS, Li Y, Banerjee S, Padhye S, Sarkar FH (2012) Hypoxia induced aggressiveness of prostate cancer cells is linked with deregulated expression of VEGF, IL-6 and miRNAs that are attenuated by CDF. PLoS One 7:e43726PubMedPubMedCentralCrossRefGoogle Scholar
  5. Benassi B, Flavin R, Marchionni L, Zanata S, Pan Y, Chowdhury D, Marani M, Strano S, Muti P, Blandino G, Loda M (2012) MYC is activated by USP2a-mediated modulation of microRNAs in prostate cancer. Cancer Disc 2:236–247CrossRefGoogle Scholar
  6. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D’urso L, Pagliuca A, Biffoni M, Labbaye C, Bartucci M, Muto G, Peschle C, DE Maria R (2008) The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 14:1271–1277PubMedCrossRefGoogle Scholar
  7. Brabletz S, Bajdak K, Meidhof S, Burk U, Niedermann G, Firat E, Wellner U, Dimmler A, Faller G, Schubert J, Brabletz T (2011) The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J 30:770–782PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68:7846–7854PubMedCrossRefGoogle Scholar
  9. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31:578–583PubMedCrossRefGoogle Scholar
  10. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9:582–589PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bussemakers MJ, Van Bokhoven A, Verhaegh GW, Smit FP, Karthaus HF, Schalken JA, Debruyne FM, Ru N, Isaacs WB (1999) DD3: a new prostate-specific gene, highly overexpressed in prostate cancer. Cancer Res 59:5975–5979PubMedGoogle Scholar
  12. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM (2002) Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 99:15524–15529PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cannell IG, Kong YW, Johnston SJ, Chen ML, Collins HM, Dobbyn HC, Elia A, Kress TR, Dickens M, Clemens MJ, Heery DM, Gaestel M, Eilers M, Willis AE, Bushell M (2010) p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci U S A 107:5375–5380PubMedPubMedCentralCrossRefGoogle Scholar
  14. Ceder JA, Jansson L, Ehrnstrom RA, Ronnstrand L, Abrahamsson PA (2008) The characterization of epithelial and stromal subsets of candidate stem/progenitor cells in the human adult prostate. Eur Urol 53:524–531PubMedCrossRefGoogle Scholar
  15. Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033PubMedCrossRefGoogle Scholar
  16. Choi YJ, Lin CP, Ho JJ, He X, Okada N, Bu P, Zhong Y, Kim SY, Bennett MJ, Chen C, Ozturk A, Hicks GG, Hannon GJ, He L (2011) miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 13:1353–1360PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM (2005) miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A 102:13944–13949PubMedPubMedCentralCrossRefGoogle Scholar
  18. Clape C, Fritz V, Henriquet C, Apparailly F, Fernandez PL, Iborra F, Avances C, Villalba M, Culine S, Fajas L (2009) miR-143 interferes with ERK5 signaling, and abrogates prostate cancer progression in mice. PLoS One 4:e7542PubMedPubMedCentralCrossRefGoogle Scholar
  19. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D’andrea A, Vidigal JA, Maughan WP, Ogrodowski P, Ventura A (2012) Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 8:e1002797PubMedPubMedCentralCrossRefGoogle Scholar
  20. Coppola V, Musumeci M, Patrizii M, Cannistraci A, Addario A, Maugeri-Sacca M, Biffoni M, Francescangeli F, Cordenonsi M, Piccolo S, Memeo L, Pagliuca A, Muto G, Zeuner A, DE Maria R, Bonci D (2013) BTG2 loss and miR-21 upregulation contribute to prostate cell transformation by inducing luminal markers expression and epithelial-mesenchymal transition. Oncogene 32:1843–1853PubMedCrossRefGoogle Scholar
  21. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY (2007) MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 67:8433–8438PubMedCrossRefGoogle Scholar
  22. Dahiya R, Mccarville J, Lee C, Hu W, Kaur G, Carroll P, Deng G (1997) Deletion of chromosome 11p15, p12, q22, q23-24 loci in human prostate cancer. Int J Cancer 72:283–288PubMedCrossRefGoogle Scholar
  23. Dong JT, Boyd JC, Frierson HF Jr (2001) Loss of heterozygosity at 13q14 and 13q21 in high grade, high stage prostate cancer. Prostate 49:166–171PubMedCrossRefGoogle Scholar
  24. Egidi MG, Cochetti G, Serva MR, Guelfi G, Zampini D, Mechelli L, Mearini E (2013) Circulating microRNAs and Kallikreins before and after radical prostatectomy: are they really prostate cancer markers? Biomed Res Int 2013:241780PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fan X, Chen X, Deng W, Zhong G, Cai Q, Lin T (2013) Up-regulated microRNA-143 in cancer stem cells differentiation promotes prostate cancer cells metastasis by modulating FNDC3B expression. BMC Cancer 13:61PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917PubMedCrossRefGoogle Scholar
  27. Fletcher CE, Dart DA, Sita-Lumsden A, Cheng H, Rennie PS, Bevan CL (2012) Androgen-regulated processing of the oncomir miR-27a, which targets Prohibitin in prostate cancer. Hum Mol Genet 21:3112–3127PubMedCrossRefGoogle Scholar
  28. Folini M, Gandellini P, Longoni N, Profumo V, Callari M, Pennati M, Colecchia M, Supino R, Veneroni S, Salvioni R, Valdagni R, Daidone MG, Zaffaroni N (2010) miR-21: an oncomir on strike in prostate cancer. Mol Cancer 9:12PubMedPubMedCentralCrossRefGoogle Scholar
  29. Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafre SA, Farace MG (2007) miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 282:23716–23724PubMedCrossRefGoogle Scholar
  30. Gandellini P, Folini M, Longoni N, Pennati M, Binda M, Colecchia M, Salvioni R, Supino R, Moretti R, Limonta P, Valdagni R, Daidone MG, Zaffaroni N (2009) miR-205 Exerts tumor-suppressive functions in human prostate through down-regulation of protein kinase Cepsilon. Cancer Res 69:2287–2295PubMedCrossRefGoogle Scholar
  31. Gandellini P, Profumo V, Casamichele A, Fenderico N, Borrelli S, Petrovich G, Santilli G, Callari M, Colecchia M, Pozzi S, De Cesare M, Folini M, Valdagni R, Mantovani R, Zaffaroni N (2012) MiR-205 regulates basement membrane deposition in human prostate: implications for cancer development. Cell Death Differ 19(11):1750–1760Google Scholar
  32. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10:593–601PubMedCrossRefGoogle Scholar
  33. Gronberg H (2003) Prostate cancer epidemiology. Lancet 361:859–864PubMedCrossRefGoogle Scholar
  34. Guo W, Ren D, Chen X, Tu X, Huang S, Wang M, Song L, Zou X, Peng X (2013) HEF1 promotes epithelial mesenchymal transition and bone invasion in prostate cancer under the regulation of microRNA-145. J Cell Biochem 114:1606–1615PubMedCrossRefGoogle Scholar
  35. Haese A, DE LA Taille A, VAN Poppel H, Marberger M, Stenzl A, Mulders PF, Huland H, Abbou CC, Remzi M, Tinzl M, Feyerabend S, Stillebroer AB, VAN Gils MP, Schalken JA (2008) Clinical utility of the PCA3 urine assay in European men scheduled for repeat biopsy. Eur Urol 54:1081–1088PubMedCrossRefGoogle Scholar
  36. Hagman Z, Larne O, Edsjo A, Bjartell A, Ehrnstrom RA, Ulmert D, Lilja H, Ceder Y (2010) miR-34c is downregulated in prostate cancer and exerts tumor suppressive functions. Int J Cancer 127:2768–2776PubMedCrossRefGoogle Scholar
  37. Hagman Z, Haflidadottir BS, Ansari M, Persson M, Bjartell A, Edsjo A, Ceder Y (2013a) The tumour suppressor miR-34c targets MET in prostate cancer cells. Br J Cancer 109(5):1271–1278PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hagman Z, Haflidadottir BS, Ceder JA, Larne O, Bjartell A, Lilja H, Edsjo A, Ceder Y (2013b) miR-205 negatively regulates the androgen receptor and is associated with adverse outcome of prostate cancer patients. Br J Cancer 108(8):1668–1676PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hart M, Wach S, Nolte E, Szczyrba J, Menon R, Taubert H, Hartmann A, Stoehr R, Wieland W, Grasser FA, Wullich B (2013) The proto-oncogene ERG is a target of microRNA miR-145 in prostate cancer. FEBS J 280:2105–2116PubMedCrossRefGoogle Scholar
  40. Helzer KT, Barnes HE, Day L, Harvey J, Billings PR, Forsyth A (2009) Circulating tumor cells are transcriptionally similar to the primary tumor in a murine prostate model. Cancer Res 69:7860–7866PubMedCrossRefGoogle Scholar
  41. Hessels D, Klein Gunnewiek JM, Van Oort I, Karthaus HF, Van Leenders GJ, Van Balken B, Kiemeney LA, Witjes JA, Schalken JA (2003) DD3(PCA3)-based molecular urine analysis for the diagnosis of prostate cancer. Eur Urol 44:8–15; discussion 15–6PubMedCrossRefGoogle Scholar
  42. Hu J, Guo H, Li H, Liu Y, Liu J, Chen L, Zhang J, Zhang N (2012) MiR-145 regulates epithelial to mesenchymal transition of breast cancer cells by targeting Oct4. PLoS One 7:e45965PubMedPubMedCentralCrossRefGoogle Scholar
  43. Huang S, Guo W, Tang Y, Ren D, Zou X, Peng X (2012) miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells. Oncol Rep 28:1831–1837PubMedGoogle Scholar
  44. Hudson RS, Yi M, Esposito D, Glynn SA, Starks AM, Yang Y, Schetter AJ, Watkins SK, Hurwitz AA, Dorsey TH, Stephens RM, Croce CM, Ambs S (2013) MicroRNA-106b-25 cluster expression is associated with early disease recurrence and targets caspase-7 and focal adhesion in human prostate cancer. Oncogene 32:4139–4147PubMedCrossRefGoogle Scholar
  45. Hulf T, Sibbritt T, Wiklund ED, Patterson K, Song JZ, Stirzaker C, Qu W, Nair S, Horvath LG, Armstrong NJ, Kench JG, Sutherland RL, Clark SJ (2013) Epigenetic-induced repression of microRNA-205 is associated with MED1 activation and a poorer prognosis in localized prostate cancer. Oncogene 32:2891–2899PubMedCrossRefGoogle Scholar
  46. Hyytinen ER, Frierson HF Jr, Boyd JC, Chung LW, Dong JT (1999) Three distinct regions of allelic loss at 13q14, 13q21-22, and 13q33 in prostate cancer. Genes Chromosomes Cancer 25:108–14cPubMedCrossRefGoogle Scholar
  47. Jain AK, Allton K, Iacovino M, Mahen E, Milczarek RJ, Zwaka TP, Kyba M, Barton MC (2012) p53 regulates cell cycle and microRNAs to promote differentiation of human embryonic stem cells. PLoS Biol 10:e1001268PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jalava SE, Urbanucci A, Latonen L, Waltering KK, Sahu B, Janne OA, Seppala J, Lahdesmaki H, Tammela TLJ, Visakorpi T (2012) Androgen-regulated miR-32 targets BTG2 and is overexpressed in castration-resistant prostate cancer. Oncogene 31:4460–4471PubMedCrossRefGoogle Scholar
  49. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ (2008) Cancer statistics, 2008. CA Cancer J Clin 58:71–96PubMedCrossRefGoogle Scholar
  50. Jenster G (1999) The role of the androgen receptor in the development and progression of prostate cancer. Semin Oncol 26:407–421PubMedGoogle Scholar
  51. Kasahara K, Taguchi T, Yamasaki I, Kamada M, Yuri K, Shuin T (2002) Detection of genetic alterations in advanced prostate cancer by comparative genomic hybridization. Cancer Genet Cytogenet 137:59–63PubMedCrossRefGoogle Scholar
  52. Kashat M, Azzouz L, Sarkar SH, Kong D, Li Y, Sarkar FH (2012) Inactivation of AR and Notch-1 signaling by miR-34a attenuates prostate cancer aggressiveness. Am J Transl Res 4:432–442PubMedPubMedCentralGoogle Scholar
  53. Kent OA, Chivukula RR, Mullendore M, Wentzel EA, Feldmann G, Lee KH, Liu S, Leach SD, Maitra A, Mendell JT (2010) Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev 24:2754–2759PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 106:405–413PubMedCrossRefGoogle Scholar
  55. Kong D, Li Y, Wang Z, Banerjee S, Ahmad A, Kim HR, Sarkar FH (2009) miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 27:1712–1721PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kong D, Heath E, Chen W, Cher M, Powell I, Heilbrun L, Li Y, Ali S, Sethi S, Hassan O, Hwang C, Gupta N, Chitale D, Sakr WA, Menon M, Sarkar FH (2012) Epigenetic silencing of miR-34a in human prostate cancer cells and tumor tissue specimens can be reversed by BR-DIM treatment. Am J Transl Res 4:14–23PubMedPubMedCentralGoogle Scholar
  57. Larne O, Martens-Uzunova E, Hagman Z, Edsjo A, Lippolis G, Den Berg MS, Bjartell A, Jenster G, Ceder Y (2013) MiQ-a novel microRNA based diagnostic and prognostic tool for prostate cancer. Int J Cancer 132(12):2867–2875Google Scholar
  58. Lee SO, Ma Z, Yeh CR, Luo J, Lin TH, Lai KP, Yamashita S, Liang L, Tian J, Li L, Jiang Q, Huang CK, Niu Y, Yeh S, Chang C (2013) New therapy targeting differential androgen receptor signaling in prostate cancer stem/progenitor vs. non-stem/progenitor cells. J Mol Cell Biol 5:14–26PubMedCrossRefGoogle Scholar
  59. Leite KR, Tomiyama A, Reis ST, Sousa-Canavez JM, Sanudo A, Camara-Lopes LH, Srougi M (2013) MicroRNA expression profiles in the progression of prostate cancer-from high-grade prostate intraepithelial neoplasia to metastasis. Urol Oncol 31(6):796–801Google Scholar
  60. Leong KG, Wang BE, Johnson L, Gao WQ (2008) Generation of a prostate from a single adult stem cell. Nature 456:804–808PubMedCrossRefGoogle Scholar
  61. Lin PC, Chiu YL, Banerjee S, Park K, Mosquera JM, Giannopoulou E, Alves P, Tewari AK, Gerstein MB, Beltran H, Melnick AM, Elemento O, Demichelis F, Rubin MA (2013) Epigenetic repression of miR-31 disrupts androgen receptor homeostasis and contributes to prostate cancer progression. Cancer Res 73:1232–1244PubMedCrossRefGoogle Scholar
  62. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG (2011a) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 17:211–215PubMedPubMedCentralCrossRefGoogle Scholar
  63. Liu LZ, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung HF, Lai L, Jiang BH (2011b) MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1alpha expression. PLoS One 6:e19139PubMedPubMedCentralCrossRefGoogle Scholar
  64. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, Yi M, Stephens RM, Seng V, Sheppard-Tillman H, Martin P, Kelly K (2013) MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 32:296–306PubMedCrossRefGoogle Scholar
  65. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR (2005) MicroRNA expression profiles classify human cancers. Nature 435:834–838PubMedCrossRefGoogle Scholar
  66. Majid S, Dar AA, Saini S, Yamamura S, Hirata H, Tanaka Y, Deng G, Dahiya R (2010) MicroRNA-205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 116:5637–5649PubMedPubMedCentralCrossRefGoogle Scholar
  67. Majid S, Dar AA, Saini S, Shahryari V, Arora S, Zaman MS, Chang I, Yamamura S, Tanaka Y, Chiyomaru T, Deng G, Dahiya R (2013) miRNA-34b inhibits prostate cancer through demethylation, active chromatin modifications, and AKT pathways. Clin Cancer Res 19:73–84PubMedCrossRefGoogle Scholar
  68. Marks LS, Fradet Y, Deras IL, Blase A, Mathis J, Aubin SM, Cancio AT, Desaulniers M, Ellis WJ, Rittenhouse H, Groskopf J (2007) PCA3 molecular urine assay for prostate cancer in men undergoing repeat biopsy. Urology 69:532–535PubMedCrossRefGoogle Scholar
  69. Martens-Uzunova ES, Jalava SE, Dits NF, VAN Leenders GJLH, Moller S, Trapman J, Bangma CH, Litman T, Visakorpi T, Jenster G (2012) Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer. Oncogene 31:978–991PubMedCrossRefGoogle Scholar
  70. Mattie MD, Benz CC, Bowers J, Sensinger K, Wong L, Scott GK, Fedele V, Ginzinger D, Getts R, Haqq C (2006) Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Mol Cancer 5:24PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mishra S, Deng JJ, Gowda PS, Rao MK, Lin CL, Chen CL, Huang T, Sun LZ (2014) Androgen receptor and microRNA-21 axis downregulates transforming growth factor beta receptor II (TGFBR2) expression in prostate cancer. Oncogenesis 33(31):4097–4106Google Scholar
  72. Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, Colarossi C, Francescangeli F, Biffoni M, Collura D, Giacobbe A, D’urso L, Falchi M, Venneri MA, Muto G, DE Maria R, Bonci D (2011) Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene 30:4231–4242PubMedCrossRefGoogle Scholar
  73. Narayanan R, Jiang J, Gusev Y, Jones A, Kearbey JD, Miller DD, Schmittgen TD, Dalton JT (2010) MicroRNAs are mediators of androgen action in prostate and muscle. PLoS One 5:e13637PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ostling P, Leivonen SK, Aakula A, Kohonen P, Makela R, Hagman Z, Edsjo A, Kangaspeska S, Edgren H, Nicorici D, Bjartell A, Ceder Y, Perala M, Kallioniemi O (2011) Systematic analysis of microRNAs targeting the androgen receptor in prostate cancer cells. Cancer Res 71:1956–1967PubMedCrossRefGoogle Scholar
  75. Ozen M, Creighton CJ, Ozdemir M, Ittmann M (2008) Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 27:1788–1793PubMedCrossRefGoogle Scholar
  76. Peng X, Guo W, Liu T, Wang X, Tu X, Xiong D, Chen S, Lai Y, Du H, Chen G, Liu G, Tang Y, Huang S, Zou X (2011) Identification of miRs-143 and -145 that is associated with bone metastasis of prostate cancer and involved in the regulation of EMT. PLoS One 6:e20341PubMedPubMedCentralCrossRefGoogle Scholar
  77. Piovan C, Palmieri D, DI Leva G, Braccioli L, Casalini P, Nuovo G, Tortoreto M, Sasso M, Plantamura I, Triulzi T, Taccioli C, Tagliabue E, Iorio MV, Croce CM (2012) Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol Oncol 6:458–472PubMedPubMedCentralCrossRefGoogle Scholar
  78. Ploussard G, Durand X, Xylinas E, Moutereau S, Radulescu C, Forgue A, Nicolaiew N, Terry S, Allory Y, Loric S, Salomon L, Vacherot F, DE LA Taille A (2011) Prostate cancer antigen 3 score accurately predicts tumour volume and might help in selecting prostate cancer patients for active surveillance. Eur Urol 59:422–429PubMedCrossRefGoogle Scholar
  79. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465:1033–1038PubMedPubMedCentralCrossRefGoogle Scholar
  80. Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, Visakorpi T (2007) MicroRNA expression profiling in prostate cancer. Cancer Res 67:6130–6135PubMedCrossRefGoogle Scholar
  81. Porkka KP, Ogg EL, Saramaki OR, Vessella RL, Pukkila H, Lahdesmaki H, VAN Weerden WM, Wolf M, Kallioniemi OP, Jenster G, Visakorpi T (2011) The miR-15a-miR-16-1 locus is homozygously deleted in a subset of prostate cancers. Genes Chromosomes Cancer 50:499–509PubMedCrossRefGoogle Scholar
  82. Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M (2012) Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res 5:492–497CrossRefGoogle Scholar
  83. Prueitt RL, Yi M, Hudson RS, Wallace TA, Howe TM, Yfantis HG, Lee DH, Stephens RM, Liu CG, Calin GA, Croce CM, Ambs S (2008) Expression of microRNAs and protein-coding genes associated with perineural invasion in prostate cancer. Prostate 68(11):1152–1164PubMedPubMedCentralCrossRefGoogle Scholar
  84. Puhr M, Hoefer J, Schafer G, Erb HH, Oh SJ, Klocker H, Heidegger I, Neuwirt H, Culig Z (2012) Epithelial-to-mesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205. Am J Pathol 181:2188–2201PubMedCrossRefGoogle Scholar
  85. Qu F, Cui X, Hong Y, Wang J, Li Y, Chen L, Liu Y, Gao Y, Xu D, Wang Q (2013a) MicroRNA-185 suppresses proliferation, invasion, migration, and tumorigenicity of human prostate cancer cells through targeting androgen receptor. Mol Cell Biochem 377:121–130PubMedCrossRefGoogle Scholar
  86. Qu Y, Li WC, Hellem MR, Rostad K, Popa M, Mccormack E, Oyan AM, Kalland KH, Ke XS (2013b) MiR-182 and miR-203 induce mesenchymal to epithelial transition and self-sufficiency of growth signals via repressing SNAI2 in prostate cells. Int J Cancer 133:544–555PubMedCrossRefGoogle Scholar
  87. Reis ST, Pontes-Junior J, Antunes AA, Dall’Oglio MF, Dip N, Passerotti CC, Rossini GA, Morais DR, Nesrallah AJ, Piantino C, Srougi M, Leite KR (2012) miR-21 may acts as an oncomir by targeting RECK, a matrix metalloproteinase regulator, in prostate cancer. BMC Urol 12:14PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ren D, Wang M, Guo W, Zhao X, Tu X, Huang S, Zou X, Peng X (2013) Wild-type p53 suppresses the epithelial-mesenchymal transition and stemness in PC-3 prostate cancer cells by modulating miR145. Int J Oncol 42:1473–1481PubMedGoogle Scholar
  89. Ribas J, Ni X, Haffner M, Wentzel EA, Salmasi AH, Chowdhury WH, Kudrolli TA, Yegnasubramanian S, Luo J, Rodriguez R, Mendell JT, Lupold SE (2009) miR-21: an androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res 69:7165–7169PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, Kumar S, Elble R, Watabe K, Mo YY (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A 106:3207–3212PubMedPubMedCentralCrossRefGoogle Scholar
  91. Schubert M, Spahn M, Kneitz S, Scholz CJ, Joniau S, Stroebel P, Riedmiller H, Kneitz B (2013) Distinct microRNA expression profile in prostate cancer patients with early clinical failure and the impact of let-7 as prognostic marker in high-risk prostate cancer. PLoS One 8:e65064PubMedPubMedCentralCrossRefGoogle Scholar
  92. Shen J, Hruby GW, Mckiernan JM, Gurvich I, Lipsky MJ, Benson MC, Santella RM (2012) Dysregulation of circulating microRNAs and prediction of aggressive prostate cancer. Prostate 72:1469–1477PubMedPubMedCentralCrossRefGoogle Scholar
  93. Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, Devere White RW (2007) An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci U S A 104:19983–19988PubMedPubMedCentralCrossRefGoogle Scholar
  94. Shi XB, Xue L, Ma AH, Tepper CG, Kung HJ, White RW (2011) miR-125b promotes growth of prostate cancer xenograft tumor through targeting pro-apoptotic genes. Prostate 71:538–549PubMedCrossRefGoogle Scholar
  95. Shi XB, Xue L, Ma AH, Tepper CG, Gandour-Edwards R, Kung HJ, Devere White RW (2013) Tumor suppressive miR-124 targets androgen receptor and inhibits proliferation of prostate cancer cells. Oncogene 32:4130–4138PubMedCrossRefGoogle Scholar
  96. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, Hermeking H (2011) miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10:4256–4271PubMedCrossRefGoogle Scholar
  97. Slabakova E, Pernicova Z, Slavickova E, Starsichova A, Kozubik A, Soucek K (2011) TGF-beta1-induced EMT of non-transformed prostate hyperplasia cells is characterized by early induction of SNAI2/slug. Prostate 71:1332–1343PubMedGoogle Scholar
  98. Suh SO, Chen Y, Zaman MS, Hirata H, Yamamura S, Shahryari V, Liu J, Tabatabai ZL, Kakar S, Deng G, Tanaka Y, Dahiya R (2011) MicroRNA-145 is regulated by DNA methylation and p53 gene mutation in prostate cancer. Carcinogenesis 32:772–778PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sun Y, Wang BE, Leong KG, Yue P, Li L, Jhunjhunwala S, Chen D, Seo K, Modrusan Z, Gao WQ, Settleman J, Johnson L (2012) Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res 72:527–536PubMedCrossRefGoogle Scholar
  100. Sun T, Wang X, He HH, Sweeney CJ, Liu SX, Brown M, Balk S, Lee GS, Kantoff PW (2014) MiR-221 promotes the development of androgen independence in prostate cancer cells via downregulation of HECTD2 and RAB1A. Oncogenesis 33(21):2790–2800Google Scholar
  101. Szczyrba J, Loprich E, Wach S, Jung V, Unteregger G, Barth S, Grobholz R, Wieland W, Stohr R, Hartmann A, Wullich B, Grasser F (2010) The microRNA profile of prostate carcinoma obtained by deep sequencing. Mol Cancer Res 8:529–538PubMedCrossRefGoogle Scholar
  102. Takeshita F, Patrawala L, Osaki M, Takahashi RU, Yamamoto Y, Kosaka N, Kawamata M, Kelnar K, Bader AG, Brown D, Ochiya T (2010) Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol Ther 18:181–187PubMedCrossRefGoogle Scholar
  103. Tao J, Wu D, Xu B, Qian W, Li P, Lu Q, Yin C, Zhang W (2012) microRNA-133 inhibits cell proliferation, migration and invasion in prostate cancer cells by targeting the epidermal growth factor receptor. Oncol Rep 27:1967–1975PubMedGoogle Scholar
  104. Tian B, Hu J, Zhang H, Lutz CS (2005) A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res 33:201–212PubMedPubMedCentralCrossRefGoogle Scholar
  105. Tong AW, Fulgham P, Jay C, Chen P, Khalil I, Liu S, Senzer N, Eklund AC, Han J, Nemunaitis J (2009) MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther 16(3):206–216Google Scholar
  106. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, Tokino T (2008) Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 68:4123–4132PubMedCrossRefGoogle Scholar
  107. Tucci P, Agostini M, Grespi F, Markert EK, Terrinoni A, Vousden KH, Muller PA, Dotsch V, Kehrloesser S, Sayan BS, Giaccone G, Lowe SW, Takahashi N, Vandenabeele P, Knight RA, Levine AJ, Melino G (2012) Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer. Proc Natl Acad Sci U S A 109:15312–15317PubMedPubMedCentralCrossRefGoogle Scholar
  108. Vallejo DM, Caparros E, Dominguez M (2011) Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells. EMBO J 30:756–769PubMedPubMedCentralCrossRefGoogle Scholar
  109. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, IORIO M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103:2257–2261PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wach S, Nolte E, Szczyrba J, Stohr R, Hartmann A, Orntoft T, Dyrskjot L, Eltze E, Wieland W, Keck B, Ekici AB, Grasser F, Wullich B (2012) MicroRNA profiles of prostate carcinoma detected by multiplatform microRNA screening. Int J Cancer 130:611–621PubMedCrossRefGoogle Scholar
  111. Wang L, Tang H, Thayanithy V, Subramanian S, Oberg AL, Cunningham JM, Cerhan JR, Steer CJ, Thibodeau SN (2009) Gene networks and microRNAs implicated in aggressive prostate cancer. Cancer Res 69:9490–9497PubMedPubMedCentralCrossRefGoogle Scholar
  112. Watahiki A, Macfarlane RJ, Gleave ME, Crea F, Wang Y, Helgason CD, Chi KN (2013) Plasma miRNAs as biomarkers to identify patients with castration-resistant metastatic prostate cancer. Int J Mol Sci 14:7757–7770PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wiklund ED, Bramsen JB, Hulf T, Dyrskjot L, Ramanathan R, Hansen TB, Villadsen SB, Gao S, Ostenfeld MS, Borre M, Peter ME, Orntoft TF, Kjems J, Clark SJ (2011) Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer J Int Cancer 128:1327–1334CrossRefGoogle Scholar
  114. Wu H, Zhu S, Mo YY (2009) Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19:439–448PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wu D, Huang P, Wang L, Zhou Y, Pan H, Qu P (2013) MicroRNA-143 inhibits cell migration and invasion by targeting matrix metalloproteinase 13 in prostate cancer. Mol Med Rep 8(2):626–630PubMedGoogle Scholar
  116. Xiao J, Gong AY, Eischeid AN, Chen D, Deng C, Young CY, Chen XM (2012) miR-141 modulates androgen receptor transcriptional activity in human prostate cancer cells through targeting the small heterodimer partner protein. Prostate 72:1514–1522PubMedCrossRefGoogle Scholar
  117. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137:647–658PubMedCrossRefGoogle Scholar
  118. Xu B, Niu X, Zhang X, Tao J, Wu D, Wang Z, Li P, Zhang W, Wu H, Feng N, Hua L, Wang X (2011) miR-143 decreases prostate cancer cells proliferation and migration and enhances their sensitivity to docetaxel through suppression of KRAS. Mol Cell Biochem 350:207–213PubMedCrossRefGoogle Scholar
  119. Yamakuchi M, Lowenstein CJ (2009) MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 8:712–715PubMedCrossRefGoogle Scholar
  120. Yamamura S, Saini S, Majid S, Hirata H, Ueno K, Deng G, Dahiya R (2012) MicroRNA-34a modulates c-Myc transcriptional complexes to suppress malignancy in human prostate cancer cells. PLoS One 7:e29722PubMedPubMedCentralCrossRefGoogle Scholar
  121. Yaman Agaoglu F, Kovancilar M, Dizdar Y, Darendeliler E, Holdenrieder S, Dalay N, Gezer U (2011) Investigation of miR-21, miR-141, and miR-221 in blood circulation of patients with prostate cancer. Tumour Biol: J Int Soc Oncol Dev Biol Med 32:583–588CrossRefGoogle Scholar
  122. Yang X, Bemis L, Su LJ, Gao D, Flaig TW (2012) miR-125b regulation of androgen receptor signaling via modulation of the receptor complex co-repressor NCOR2. BioRes Open Access 1:55–62PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zaman MS, Chen Y, Deng G, Shahryari V, Suh SO, Saini S, Majid S, Liu J, Khatri G, Tanaka Y, Dahiya R (2010) The functional significance of microRNA-145 in prostate cancer. Br J Cancer 103:256–264PubMedPubMedCentralCrossRefGoogle Scholar
  124. Zhang L, Zhao W, Valdez JM, Creighton CJ, Xin L (2010) Low-density Taqman miRNA array reveals miRNAs differentially expressed in prostatic stem cells and luminal cells. Prostate 70:297–304PubMedPubMedCentralGoogle Scholar
  125. Zhang HL, Yang LF, Zhu Y, Yao XD, Zhang SL, Dai B, Zhu YP, Shen YJ, Shi GH, Ye DW (2011) Serum miRNA-21: elevated levels in patients with metastatic hormone-refractory prostate cancer and potential predictive factor for the efficacy of docetaxel-based chemotherapy. Prostate 71:326–331PubMedCrossRefGoogle Scholar
  126. Zheng C, Yinghao S, Li J (2012) MiR-221 expression affects invasion potential of human prostate carcinoma cell lines by targeting DVL2. Med Oncol 29:815–822PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Translational Cancer ResearchLund UniversityLundSweden

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