Clinical and Translational Oncology

, Volume 14, Issue 11, pp 803–811

miRNAs as biomarkers in prostate cancer

  • Irene Casanova-Salas
  • José Rubio-Briones
  • Antonio Fernández-Serra
  • Jose Antonio López-Guerrero
Educational Series - Blue Series Advances in Translational Oncology

Abstract

Current prostate cancer (PCa) diagnosis is based in the serum prostate-specific antigen biomarker and digital rectal examination. However, these methods are limited by a low predictive value (24–37 %) and a high risk of mistaken results. During last years, new promising biomarkers such as Prostate Cancer Antigen 3 (PCA-3) and TMPRSS2-ETS fusion genes have been evaluated for their clinical use. However, the search of new biomarkers that could be used for PCa diagnosis and prognosis is still needed. Recent studies have demonstrated that the aberrant expression of microRNAs (miRNAs), small non-coding RNAs that negatively regulate gene expression, is related with the development of several cancers, including PCa. Since miRNAs serve as phenotypic signatures of different cancers, they appear as potential diagnostic, prognostic and therapeutic tools. Here, we review the current knowledge of miRNA expression patterns in PCa and their role in PCa prognosis and therapeutics.

Keywords

Prostate cancer Biomarker MicroRNA 

References

  1. 1.
    Fernández-Serra A, Rubio-Briones J, García-Casado Z, Solsona E, López-Guerrero JA (2011) Cáncer de próstata: la revolución de los genes de fusión. Act Urol Esp 35:420–428Google Scholar
  2. 2.
    Bunting PS (2002) Screening for prostate cancer with prostate-specific antigen: beware the biases. Clin Chim Acta 315:71–97PubMedGoogle Scholar
  3. 3.
    Thompson IM, Ankerst DP, Chi C, Goodman PJ, Tangen CM et al (2006) Assessing prostate cancer risk: results from the prostate cancer prevention trial. Cancer 78229:529–534Google Scholar
  4. 4.
    Stamey TA, Yang N, Hay AR, McNeal JE, Freiha FS et al (1987) Prostate-specific antigen as a serum marker for adenocarcinoma of the prostate. N Engl J Med 317:909–916PubMedGoogle Scholar
  5. 5.
    Tricoli JV, Schoenfeldt M, Conley BA (2004) Detection of prostate cancer and predicting progression: current and future diagnostic markers. Clin Cancer Res 10:3943–3953PubMedGoogle Scholar
  6. 6.
    Schröder FH, van der Cruijsen-Koeter I, de Koning HJ, Vis AN, Hoedemaeker RF et al (2000) Prostate cancer detection at low prostate specific antigen. J Urol 163:806–812PubMedGoogle Scholar
  7. 7.
    Rubio-Briones J, Fernández-Serra A, Ramírez M, Rubio L, Collado A et al (2011) Resultados del uso expandido del PCA3 score en una población española con sospecha de cáncer de próstata. Act Urol Esp 35:589–596Google Scholar
  8. 8.
    Salagierski M, Schalken JA (2012) Molecular diagnosis of prostate cancer: PCA3 and TMPRSS2:ERG gene fusion. J Urol 187:795–801PubMedGoogle Scholar
  9. 9.
    Ryan BM, Robles AI, Harris CC (2010) Genetic variation in microRNA. Nat Rev Cancer 10:389–402PubMedGoogle Scholar
  10. 10.
    Pang Y, Young CYF, Yuan H (2010) MicroRNAs and prostate cancer. Acta Biochim Biophys Hung 42:363–369Google Scholar
  11. 11.
    Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S et al (2002) Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. PNAS 99:13–18Google Scholar
  12. 12.
    Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL (2007) MicroRNA expression profiling in prostate cancer. Cancer Res 67:6130–6135PubMedGoogle Scholar
  13. 13.
    Saini S, Majid S, Dahiya R (2010) Diet, microRNAs and prostate cancer. Pharm Res 27:1014–1026PubMedGoogle Scholar
  14. 14.
    Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6:259–269PubMedGoogle Scholar
  15. 15.
    Karube Y, Tanaka H, Osada H, Tomida S, Tatematsu Y et al (2005) Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci 96:111–115PubMedGoogle Scholar
  16. 16.
    Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M et al (2005) miR-15 and miR-16 induce apoptosis by targeting BCL2. PNAS 102:13944–13949PubMedGoogle Scholar
  17. 17.
    Volinia S, Calin GA, Liu C-gong, Ambs S, Cimmino A et al (2005) A microRNA expression signature of human solid tumors defines cancer gene targets. PNAS 103:2257–2261Google Scholar
  18. 18.
    Lu J, Getz G, Miska EA, Alvarez-saavedra E, Lamb J et al (2005) MicroRNA expression profiles classify human cancers. Nature 435:834–838PubMedGoogle Scholar
  19. 19.
    Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R et al (2005) RAS is regulated by the let-7 MicroRNA family. Cell 120:635–647PubMedGoogle Scholar
  20. 20.
    Michael MZ, Connor SMO, Pellekaan NGVH, Young GP, James RJ (2003) Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 1:882–891PubMedGoogle Scholar
  21. 21.
    Ciafrè SA, Galardi S, Mangiola A, Ferracin M, Liu C-G et al (2005) Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334:1351–1358PubMedGoogle Scholar
  22. 22.
    Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033PubMedGoogle Scholar
  23. 23.
    Eis PS, Tam W, Sun L, Chadburn A, Li Z et al (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Synthesis 102:3627–3632Google Scholar
  24. 24.
    Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H et al (2006) Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25(17):2537–2545PubMedGoogle Scholar
  25. 25.
    Zhang B, Pan X, Cobb GP, Anderson TA (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302:1–12PubMedGoogle Scholar
  26. 26.
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK et al (2008) Circulating microRNAs as stable blood-based markers for cancer detection. PNAS 105:10513–10518PubMedGoogle Scholar
  27. 27.
    Lodes MJ, Caraballo M, Suciu D, Munro S, Kumar A et al (2009) Detection of cancer with serum miRNAs on an oligonucleotide microarray. PLoS One 4:e6229PubMedGoogle Scholar
  28. 28.
    Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH et al (2010) The microRNA spectrum in 12 body fluids. Clin Chem 56:1733–1741PubMedGoogle Scholar
  29. 29.
    X-bao Shi, Xue L, Yang J, Ma A-H, Zhao J et al (2007) An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. PNAS 104:19983–19988Google Scholar
  30. 30.
    Ribas J, Ni X, Haffner M, Wentzel EA, Salmasi AH et al (2009) miR-21: an androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res 69:7165–7169PubMedGoogle Scholar
  31. 31.
    Catto JWF, Alcaraz A, Bjartell AS, Vere RD, Evans CP et al (2011) MicroRNA in prostate, bladder, and kidney cancer: a systematic review. Eur Urol 59:671–681PubMedGoogle Scholar
  32. 32.
    Epis MR, Giles KM, Barker A, Kendrick TS, Leedman PJ (2009) miR-331-3p regulates ERBB-2 expression and androgen receptor signaling in prostate cancer. J Biol Chem 284:24696–24704PubMedGoogle Scholar
  33. 33.
    White RW, Vinall RL, Tepper CG, Shi X-B (2010) MicroRNAs and their potential for translation in prostate cancer. Urol Oncol 27:307–311Google Scholar
  34. 34.
    Brase JC, Johannes M, Schlomm T, Fälth M, Haese A et al (2011) Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 128:608–616PubMedGoogle Scholar
  35. 35.
    Zaman MS, Chen Y, Deng G, Shahryari V, Suh SO et al (2010) The functional significance of microRNA-145 in prostate cancer. Br J Cancer 103:256–264PubMedGoogle Scholar
  36. 36.
    Watahiki A, Wang Y, Morris J, Dennis K, Dwyer HMO et al (2011) MicroRNAs associated with metastatic prostate cancer. PLoS One 6:e24950PubMedGoogle Scholar
  37. 37.
    Szczyrba J, Löprich E, Wach S (2010) The microRNA profile of prostate carcinoma obtained by deep sequencing. Mol Cancer Res 8:529–538PubMedGoogle Scholar
  38. 38.
    Peng X, Guo W, Liu T, Wang X, Tu X et al (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:e20341PubMedGoogle Scholar
  39. 39.
    Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM et al (2008) Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68:6162–6170PubMedGoogle Scholar
  40. 40.
    Tong AW, Fulgham P, Jay C, Chen P, Khalil I et al (2009) MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther 16:206–216PubMedGoogle Scholar
  41. 41.
    Saini S, Majid S, Yamamura S (2011) Regulatory role of mir-203 in prostate cancer progression and metastasis. Clin Cancer Res 17:5287–5298PubMedGoogle Scholar
  42. 42.
    Wang L, Tang H, Thayanithy V, Subramanian S, Oberg AL et al (2010) Gene networks and microRNAs implicated in aggressive prostate cancer. Cancer Res 69:9490–9497Google Scholar
  43. 43.
    Bex A (2011) Translating translational repression: evolving possibilities in uro-oncology. Eur Urol 59:682–683PubMedGoogle Scholar
  44. 44.
    Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R et al (2005) Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310:644–648PubMedGoogle Scholar
  45. 45.
    Rubio-Briones J, Fernández-Serra A, Calatrava A, García-Casado Z, Rubio L et al (2010) Clinical implications of TMPRSS2-ERG gene fusion expression in patients with prostate cancer treated with radical prostatectomy. J Urol 183:2054–2061PubMedGoogle Scholar
  46. 46.
    Gordanpour A, Stanimirovic A, Nam RK, Moreno CS, Sherman C et al (2011) miR-221 Is down-regulated in TMPRSS2:ERG fusion-positive prostate cancer. Anticancer Res 31:403–410PubMedGoogle Scholar
  47. 47.
    Kota J, Chivukula RR, O’Donnell KA, Wentzel EA, Montgomery CL et al (2009) Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137:1005–1017PubMedGoogle Scholar
  48. 48.
    Bhardwaj A, Singh S, Singh AP (2010) MicroRNA-based cancer therapeutics: big hope from small RNAs. Mol Cell Pharmacol 2:213–219PubMedGoogle Scholar
  49. 49.
    Si M-L, Zhu S, Wu H, Lu Z, Wu F et al (2007) miR-21-mediated tumor growth. Oncogene 26:2799–2803PubMedGoogle Scholar
  50. 50.
    Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T et al (2005) Silencing of microRNAs in vivo with “antagomirs”. Nature 438:685–689PubMedGoogle Scholar
  51. 51.
    Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721–726PubMedGoogle Scholar
  52. 52.
    Gumireddy K, Young DD, Xiong X, Hogenesch JB, Huang Q et al (2008) Small-molecule inhibitors of microrna miR-21 function. Angew Chem Int Ed Engl 47:7482–7484PubMedGoogle Scholar
  53. 53.
    Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A et al (2006) MicroRNA fingerprints during human megakaryocytopoiesis. PNAS 103:5078–5083PubMedGoogle Scholar
  54. 54.
    Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS et al (2010) Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 3:ra29PubMedGoogle Scholar
  55. 55.
    Schaefer A, Jung M, Mollenkopf H-J, Wagner I, Stephan C et al (2010) Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer 1176:1166–1176Google Scholar
  56. 56.
    Bhatnagar N, Li X, Padi SKR, Zhang Q, Tang M-S et al (2010) Downregulation of miR-205 and miR-31 confers resistance to chemotherapy-induced apoptosis in prostate cancer cells. Cell Death Dis 9:e105Google Scholar
  57. 57.
    Hermeking H (2009) The miR-34 family in cancer and apoptosis. Cell Death Differ 17:193–199PubMedGoogle Scholar
  58. 58.
    Guttilla IK, White BA (2009) Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 284:23204–23216PubMedGoogle Scholar
  59. 59.
    Mihelich BL, Khramtsova EA, Arva N, Vaishnav A, Johnson DN et al (2011) miR-183-96-182 cluster is overexpressed in prostate tissue and regulates zinc homeostasis in prostate cells. J Biol Chem 286:44503–44511PubMedGoogle Scholar
  60. 60.
    Shi X-B, Xue L, Ma A-H, Tepper CG, Kung H-J et al (2011) miR-125b promotes growth of prostate cancer xenograft tumor through targeting pro-apoptotic genes. Prostate 71:538–549PubMedGoogle Scholar
  61. 61.
    Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C et al (2004) A combined computational-experimental approach predicts human microRNA targets. Genes Dev 18:1165–1178PubMedGoogle Scholar
  62. 62.
    Fujita Y, Kojima K, Ohhashi R, Hamada N, Nozawa Y et al (2010) MiR-148a attenuates paclitaxel resistance of hormone-refractory, drug-resistant prostate cancer PC3 cells by regulating MSK1 expression. J Biol Chem 285:19076–19084PubMedGoogle Scholar
  63. 63.
    Murata T, Takayama K, Katayama S, Urano T, Horie-Inoue K et al (2010) miR-148a is an androgen-responsive microRNA that promotes LNCaP prostate cell growth by repressing its target CAND1 expression. Prostate Cancer Prostatic Dis 13:356–361PubMedGoogle Scholar
  64. 64.
    Prueitt RL, Yi M, Hudson RS, Wallace TA, Howe TM et al (2008) Expression of microRNAs and protein-coding genes associated with perineural invasion in prostate cancer. Prostate 68:1152–1164PubMedGoogle Scholar
  65. 65.
    Schnall-Levin M, Rissland OS, Johnston W, Perrimon N, Bartel DP et al (2011) Unusually effective microRNA targeting within repeat-rich coding regions of mammalian mRNAs. Genome Res 21:1395–1403PubMedGoogle Scholar
  66. 66.
    Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P et al (2011) miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 41:210–220PubMedGoogle Scholar
  67. 67.
    Barron N, Keenan J, Gammell P, Martinez VG, Freeman A et al (2011) Biochemical relapse following radical prostatectomy and miR-200a levels in prostate cancer. Prostate. doi:10.1002/pros.22469 PubMedGoogle Scholar
  68. 68.
    Su J, Zhang A, Shi Z, Ma F, Pu P et al (2011) MicroRNA-200a suppresses the Wnt/β-catenin signaling pathway by interacting with β-catenin. Int J Oncol 40:1162–1170PubMedGoogle Scholar
  69. 69.
    Eades G, Yao Y, Yang M, Zhang Y, Chumsri S et al (2011) MiR-200a regulates SIRT1 and EMT-like transformation in mammary epithelial cells. J Biol Chem 286:25992–26002PubMedGoogle Scholar
  70. 70.
    Szczyrba J, Nolte E, Wach S, Kremmer E, Stöhr R et al (2011) Downregulation of Sec23A protein by miRNA-375 in prostate carcinoma. Mol Cancer Res 9:791–800PubMedGoogle Scholar
  71. 71.
    Vallejo DM, Caparros E (2011) Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells. EMBO J 30:756–769PubMedGoogle Scholar
  72. 72.
    Chan YC, Banerjee J, Choi SY, Sen CK (2012) miR-210: the master hypoxamir. Microcirculation 19:215–223PubMedGoogle Scholar
  73. 73.
    Derfoul A, Juan AH, Difilippantonio MJ, Palanisamy N, Ried T et al (2011) Decreased microRNA-214 levels in breast cancer cells coincides with increased cell proliferation, invasion and accumulation of the Polycomb Ezh2 methyltransferase. Carcinogenesis 32:1607–1614PubMedGoogle Scholar
  74. 74.
    Liu J, Luo X-J, Xiong A-W, Zhang Z-D, Yue S et al (2010) MicroRNA-214 promotes myogenic differentiation by facilitating exit from mitosis via down-regulation of proto-oncogene N-ras. J Biol Chem 285:26599–26607PubMedGoogle Scholar
  75. 75.
    Yang H, Kong W, He L, Zhao J-J, O’Donnell JD et al (2008) MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res 68:425–433PubMedGoogle Scholar
  76. 76.
    Leite KRM, Sousa-Canavez JM, Reis ST, Tomiyama AH, Camara-Lopes LH et al (2011) Change in expression of miR-let7c, miR-100, and miR-218 from high grade localized prostate cancer to metastasis. Urol Oncol 29:265–269PubMedGoogle Scholar
  77. 77.
    Wei J-J, Wu X, Peng Y, Shi G, Basturk O et al (2011) Regulation of HMGA1 expression by microRNA-296 affects prostate cancer growth and invasion. Clin Cancer Res 17:1297–1305PubMedGoogle Scholar
  78. 78.
    Tang J-T, Wang J-L, Du W, Hong J, Zhao S-L et al (2011) MicroRNA 345, a methylation-sensitive microRNA is involved in cell proliferation and invasion in human colorectal cancer. Carcinogenesis 32:1207–1215PubMedGoogle Scholar
  79. 79.
    Josson S, Sung S-Y, Lao K, Chung LWK, Johnstone PAS (2008) Radiation modulation of microRNA in prostate cancer cell lines. Prostate 68:1599–1606PubMedGoogle Scholar
  80. 80.
    Jia W, Eneh JO, Ratnaparkhe S, Altman MK, Murph MM (2011) MicroRNA-30c-2* expressed in ovarian cancer cells suppresses growth factor-induced cellular proliferation and downregulates the oncogene BCL9. Mol Cancer Res 9:1732–1745PubMedGoogle Scholar
  81. 81.
    Zhou H, Xu X, Xun Q, Yu D, Ling J et al (2012) microRNA-30c negatively regulates endometrial cancer cells by targeting metastasis-associated gene-1. Oncol Rep 27:807–812PubMedGoogle Scholar
  82. 82.
    Jiang J, Lee EJ, Gusev Y, Schmittgen TD (2005) Real-time expression profiling of microRNA precursors in human cancer cell lines. Nucleic Acids Res 33:5394–5403PubMedGoogle Scholar
  83. 83.
    Scott GK, Goga A, Bhaumik D, Berger CE, Sullivan CS et al (2007) Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 282:1479–1486PubMedGoogle Scholar
  84. 84.
    Lin Y, Wu J, Chen H, Mao Y, Liu Y et al (2012) Cyclin-dependent kinase 4 is a novel target in micoRNA-195-mediated cell cycle arrest in bladder cancer cells. FEBS Lett 586:442–447PubMedGoogle Scholar
  85. 85.
    Fei X, Qi M, Wu B, Song Y, Wang Y et al (2012) MicroRNA-195-5p suppresses glucose uptake and proliferation of human bladder cancer T24 cells by regulating GLUT3 expression. FEBS Lett 586:392–397PubMedGoogle Scholar
  86. 86.
    He J-F, Luo Y-M, Wan X-H, Jiang D (2011) Biogenesis of miRNA-195 and its role in biogenesis, the cell cycle, and apoptosis. J Biochem Mol Toxicol 25:404–408PubMedGoogle Scholar
  87. 87.
    Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV et al (2007) miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27kip1*. J Biol Chem 282:23716–23724PubMedGoogle Scholar
  88. 88.
    Spahn M, Kneitz S, Scholz C-J, Stenger N, Rüdiger T et al (2010) Expression of microRNA-221 is progressively reduced in aggressive prostate cancer and metastasis and predicts clinical recurrence. Int J Cancer 127:394–403PubMedGoogle Scholar
  89. 89.
    Zhang J, Zhang H, Liu J, Tu X, Zang Y et al (2012) miR-30 inhibits TGF-β1-induced epithelial-to-mesenchymal transition in hepatocyte by targeting Snail1. Biochem Biophys Res Commun 417:1100–1105PubMedGoogle Scholar
  90. 90.
    Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H et al (2011) Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer 106:405–413PubMedGoogle Scholar
  91. 91.
    Giles KM, Barker A, Zhang PM, Epis MR, Leedman PJ (2011) MicroRNA regulation of growth factor receptor signaling in human cancer cells. Methods Mol Biol 676:147–163PubMedGoogle Scholar
  92. 92.
    Takeshita F, Patrawala L, Osaki M, Takahashi R-U, Yamamoto Y et al (2010) Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol Ther 18:181–187PubMedGoogle Scholar
  93. 93.
    Gao P, Tchernyshyov I, Chang T-C, Lee Y-S, Kita K et al (2009) c-Myc suppression of miR-23 enhances mitochondrial glutaminase and glutamine metabolism. Nature 458:762–765PubMedGoogle Scholar
  94. 94.
    Fukuda Y, Kawasaki H, Taira K (2005) Exploration of human miRNA target genes in neuronal differentiation. Nucleic Acid Symp Ser 49:341–342Google Scholar
  95. 95.
    Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany AM (2010) miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285:25221–25231PubMedGoogle Scholar
  96. 96.
    Xu H, Cheung IY, Guo H-F, Cheung N-KV (2009) MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7–H3: potential implications for immune based therapy of human solid tumors. Cancer Res 69:6275–6281PubMedGoogle Scholar
  97. 97.
    Fujita Y, Kojima K, Hamada N, Ohhashi R, Akao Y et al (2008) Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells. Biochem Biophys Res Commun 377:114–119PubMedGoogle Scholar
  98. 98.
    Kojima K, Fujita Y, Nozawa Y, Deguchi T, Ito M (2010) MiR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate 70:1501–1512PubMedGoogle Scholar
  99. 99.
    Tsuchida A, Ohno S, Wu W, Borjigin N, Fujita K et al (2011) miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci 102:2264–2271PubMedGoogle Scholar
  100. 100.
    Sun D, Lee YS, Malhotra A, Kim HK, Matecic M et al (2011) miR-99 family of microRNAs suppresses the expression of prostate-specific antigen and prostate cancer cell proliferation. Cancer Res 71:1313–1324PubMedGoogle Scholar
  101. 101.
    Varambally S, Cao Q, Mani R-S, Shankar S, Wang X et al (2008) Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322:1695–1699PubMedGoogle Scholar
  102. 102.
    Wang W-X, Kyprianou N, Wang X, Nelson PT (2010) Dysregulation of the mitogen granulin in human cancer through the miR-15/107 microRNA gene group. Cancer Res 70:9137–9142PubMedGoogle Scholar
  103. 103.
    Crawford M, Brawner E, Batte K, Yu L, Hunter MG et al (2008) MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun 373:607–612PubMedGoogle Scholar
  104. 104.
    Fish JE, Santoro MM, Morton SU, Yu S, Yeh R-F et al (2008) miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 15:272–284PubMedGoogle Scholar
  105. 105.
    Musiyenko A, Bitko V, Barik S (2008) Ectopic expression of miR-126*, an intronic product of the vascular endothelial EGF-like 7 gene, regulates prostein translation and invasiveness of prostate cancer LNCaP cells. J Mol Med 86:313–322PubMedGoogle Scholar
  106. 106.
    Evangelisti C, Florian MC, Massimi I, Dominici C, Giannini G et al (2009) MiR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasiveness. FASEB J 23:4276–4287PubMedGoogle Scholar
  107. 107.
    Khan AP, Poisson LM, Bhat VB, Fermin D, Zhao R et al (2010) Quantitative proteomic profiling of prostate cancer reveals a role for miR-128 in prostate cancer. Mol Cell Proteomics 9:298–312PubMedGoogle Scholar
  108. 108.
    Clapé C, Fritz V, Henriquet C, Apparailly F, Fernandez PL et al (2009) miR-143 interferes with ERK5 signaling, and abrogates prostate cancer progression in mice. PloS One 4:e7542PubMedGoogle Scholar
  109. 109.
    Xu B, Niu X, Zhang X, Tao J, Wu D et al (2011) miR-143 decreases prostate cancer cells proliferation and migration and enhances their sensitivity to docetaxel through suppression of KRAS. Mol Cell Biochem 350:207–213PubMedGoogle Scholar
  110. 110.
    Chen Z, Zeng H, Guo Y, Liu P, Pan H et al (2010) miRNA-145 inhibits non-small cell lung cancer cell proliferation by targeting c-Myc. J Exp Clin Cancer Res 29:151PubMedGoogle Scholar
  111. 111.
    Ozen M, Creighton CJ, Ozdemir M, Ittmann M (2008) Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 27:1788–1793PubMedGoogle Scholar
  112. 112.
    S-lung L, Chiang A, Chang D, Ying S-Y (2008) Loss of mir-146a function in hormone-refractory prostate cancer. RNA 14:417–424Google Scholar
  113. 113.
    Gandellini P, Folini M, Longoni N, Colecchia M, Salvioni R et al (2009) miR-205 exerts tumor-suppressive functions in human prostate cancer through down-regulation of protein kinase Cε. Cancer Res 69:2287–2295PubMedGoogle Scholar
  114. 114.
    Majid S, Dar AA, Saini S, Yamamura S, Hirata H et al (2010) MicroRNA-205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 116:5637–5649PubMedGoogle Scholar
  115. 115.
    Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML et al (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123:819–831PubMedGoogle Scholar
  116. 116.
    Shi W, Gerster K, Alajez NM, Tsang J, Waldron L et al (2011) MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res 71:2926–2937PubMedGoogle Scholar
  117. 117.
    Bronisz A, Godlewski J, Wallace JA, Merchant AS, Nowicki MO et al (2011) Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol 14:159–167PubMedGoogle Scholar
  118. 118.
    Lee K-H, Chen Y-L, Yeh S-D, Hsiao M, Lin J-T et al (2009) MicroRNA-330 acts as tumor suppressor and induces apoptosis of prostate cancer cells through E2F1-mediated suppression of Akt phosphorylation. Oncogene 28:3360–3370PubMedGoogle Scholar
  119. 119.
    Noonan EJ, Place RF, Pookot D, Basak S, Whitson JM et al (2009) miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene 28:1714–1724PubMedGoogle Scholar

Copyright information

© Federación de Sociedades Españolas de Oncología (FESEO) 2012

Authors and Affiliations

  • Irene Casanova-Salas
    • 1
  • José Rubio-Briones
    • 2
  • Antonio Fernández-Serra
    • 1
  • Jose Antonio López-Guerrero
    • 1
  1. 1.Laboratory of Molecular BiologyFundacion Instituto Valenciano de OncologiaValenciaSpain
  2. 2.Department of UrologyFundacion Instituto Valenciano de OncologiaValenciaSpain

Personalised recommendations