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BioMed Research International
Volume 2014 (2014), Article ID 146170, 17 pages
http://dx.doi.org/10.1155/2014/146170
Review Article

MicroRNA as New Tools for Prostate Cancer Risk Assessment and Therapeutic Intervention: Results from Clinical Data Set and Patients’ Samples

1Departement of Hematology, Oncology and Molecular Medicine, Istituto Superiore Sanità, Viale Regina Elena 299, 00161 Rome, Italy
2Regina Elena National Cancer Institute, Via Fermo Ognibene, 00144 Rome, Italy

Received 6 June 2014; Revised 18 August 2014; Accepted 21 August 2014; Published 16 September 2014

Academic Editor: Paolo Gandellini

Copyright © 2014 Alessio Cannistraci et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Jemal, M. M. Center, C. DeSantis, and E. M. Ward, “Global patterns of cancer incidence and mortality rates and trends,” Cancer Epidemiology Biomarkers and Prevention, vol. 19, no. 8, pp. 1893–1907, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. C. J. Keto and S. J. Freedland, “A risk-stratified approach to prostate-specific antigen screening,” European Urology, vol. 59, no. 4, pp. 506–508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Hoffman, “Screening for prostate cancer,” New England Journal of Medicine, vol. 365, no. 21, pp. 2013–2019, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Loeb, M. A. Bjurlin, J. Nicholson et al., “Overdiagnosis and overtreatment of prostate cancer,” European Urology, vol. 65, no. 6, pp. 1046–1055, 2014. View at Publisher · View at Google Scholar
  5. L. Klotz and M. Emberton, “Management of low risk prostate cancer-active surveillance and focal therapy,” Nature Reviews Clinical Oncology, vol. 11, no. 6, pp. 324–334, 2014. View at Publisher · View at Google Scholar
  6. A. Bill-Axelson, L. Holmberg, M. Ruutu et al., “Radical prostatectomy versus watchful waiting in early prostate cancer,” The New England Journal of Medicine, vol. 364, no. 18, pp. 1708–1717, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Morris, B. Emami, P. M. Mauch et al., “Evidence-based review of three-dimensional conformal radiotherapy for localized prostate cancer: an ASTRO outcomes initiative,” International Journal of Radiation Oncology Biology Physics, vol. 62, no. 1, pp. 3–19, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. S. A. Boorjian, R. H. Thompson, M. K. Tollefson et al., “Long-term risk of clinical progression after biochemical recurrence following radical prostatectomy: the impact of time from surgery to recurrence,” European Urology, vol. 59, no. 6, pp. 893–899, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Kirby, C. Hirst, and E. D. Crawford, “Characterising the castration-resistant prostate cancer population: a systematic review,” International Journal of Clinical Practice, vol. 65, no. 11, pp. 1180–1192, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. R. W. Carthew and E. J. Sontheimer, “Origins and mechanisms of miRNAs and siRNAs,” Cell, vol. 136, no. 4, pp. 642–655, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. J. R. Lytle, T. A. Yario, and J. A. Steitz, “Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 23, pp. 9667–9672, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Tay, J. Zhang, A. M. Thomson, B. Lim, and I. Rigoutsos, “MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation,” Nature, vol. 455, no. 7216, pp. 1124–1128, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. U. A. Ørom, F. C. Nielsen, and A. H. Lund, “MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation,” Molecular Cell, vol. 30, no. 4, pp. 460–471, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. G. A. Calin, C. D. Dumitru, M. Shimizu et al., “Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15524–15529, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Sita-Lumsden, D. A. Dart, J. Waxman, and C. L. Bevan, “Circulating microRNAs as potential new biomarkers for prostate cancer,” British Journal of Cancer, vol. 108, no. 10, pp. 1925–1930, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Wang, S. K. Huang, M. Zhao et al., “Identification of a circulating MicroRNA signature for colorectal cancer detection,” PloS ONE, vol. 9, no. 4, Article ID e87451, p. 9, 2014. View at Publisher · View at Google Scholar
  17. M. T. Weigel and M. Dowsett, “Current and emerging biomarkers in breast cancer: prognosis and prediction,” Endocrine-Related Cancer, vol. 17, no. 4, pp. R245–R262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Fabbri, “MiRNAs as molecular biomarkers of cancer,” Expert Review of Molecular Diagnostics, vol. 10, no. 4, pp. 435–444, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. P. S. Mitchell, R. K. Parkin, E. M. Kroh et al., “Circulating microRNAs as stable blood-based markers for cancer detection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10513–10518, 2008. View at Publisher · View at Google Scholar
  20. J. D. Arroyo, J. R. Chevillet, E. M. Kroh et al., “Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 12, pp. 5003–5008, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. M. A. Cortez, C. Bueso-Ramos, J. Ferdin, G. Lopez-Berestein, A. K. Sood, and G. A. Calin, “MicroRNAs in body fluids—the mix of hormones and biomarkers,” Nature Reviews Clinical Oncology, vol. 8, no. 8, pp. 467–477, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Zhou, M. Y. Fong, Y. Min et al., “Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis,” Cancer Cell, vol. 25, no. 4, pp. 501–515, 2014. View at Google Scholar
  23. H. Schwarzenbach, N. Nishida, G. A. Calin, and K. Pantel, “Clinical relevance of circulating cell-free microRNAs in cancer,” Nature Reviews Clinical Oncology, vol. 11, no. 3, pp. 145–156, 2014. View at Publisher · View at Google Scholar
  24. B. S. Taylor, N. Schultz, H. Hieronymus et al., “Integrative genomic profiling of human prostate cancer,” Cancer Cell, vol. 18, no. 1, pp. 11–22, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. C. W. Brennan, R. G. Verhaak, A. McKenna et al., “The somatic genomic landscape of glioblastoma,” Cell, vol. 155, no. 2, pp. 462–477, 2013. View at Google Scholar
  26. J. Tosoian and S. Loeb, “PSA and beyond: the past, present, and future of investigative biomarkers for prostate cancer,” TheScientificWorldJournal, vol. 10, pp. 1919–1931, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Lu, G. Getz, E. A. Miska et al., “MicroRNA expression profiles classify human cancers,” Nature, vol. 435, no. 7043, pp. 834–838, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Coppola, R. de Maria, and D. Bonci, “MicroRNAs and prostate cancer,” Endocrine-Related Cancer, vol. 17, no. 1, pp. F1–F17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Y.-X. Fang and W.-Q. Gao, “Roles of microRNAs during prostatic tumorigenesis and tumor progression,” Oncogene, vol. 33, no. 2, pp. 135–147, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. I. Casanova-Salas, J. Rubio-Briones, A. Fernández-Serra, and J. A. López-Guerrero, “miRNAs as biomarkers in prostate cancer,” Clinical and Translational Oncology, vol. 14, no. 11, pp. 803–811, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Volinia, G. A. Calin, C.-G. Liu et al., “A microRNA expression signature of human solid tumors defines cancer gene targets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 7, pp. 2257–2261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Ambs, R. L. Prueitt, M. Yi et al., “Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer,” Cancer Research, vol. 68, no. 15, pp. 6162–6170, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Parikh, C. Lee, and P. Joseph, “microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial-mesenchymal transition,” Nature Communications, vol. 5, article 2977, 2014. View at Publisher · View at Google Scholar
  34. J. Brockhausen, S. S. Tay, C. A. Grzelak et al., “miR-181a mediates TGF-β-induced hepatocyte EMT and is dysregulated in cirrhosis and hepatocellular cancer,” Liver International, 2014. View at Publisher · View at Google Scholar
  35. Z. Wei, L. Cui, Z. Mei, M. Liu, and D. Zhang, “miR-181a mediates metabolic shift in colon cancer cells via the PTEN/AKT pathway,” FEBS Letters, vol. 588, no. 9, pp. 1773–1779, 2014. View at Google Scholar
  36. T. Hou, J. Ou, X. Zhao, X. Huang, Y. Huang, and Y. Zhang, “MicroRNA-196a promotes cervical cancer proliferation through the regulation of FOXO1 and p27Kip1,” British Journal of Cancer, vol. 110, no. 5, pp. 1260–1268, 2014. View at Google Scholar
  37. F. Huang, J. Tang, X. Zhuang et al., “MiR-196a promotes pancreatic cancer progression by targeting nuclear factor kappa-B-inhibitor alpha,” PLoS ONE, vol. 9, no. 2, Article ID e87897, 2014. View at Publisher · View at Google Scholar
  38. K. P. Porkka, M. J. Pfeiffer, K. K. Waltering, R. L. Vessella, T. L. J. Tammela, and T. Visakorpi, “MicroRNA expression profiling in prostate cancer,” Cancer Research, vol. 67, no. 13, pp. 6130–6135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. R. I. Aqeilan, G. A. Calin, and C. M. Croce, “miR-15a and miR-16-1 in cancer: discovery, function and future perspectives,” Cell Death and Differentiation, vol. 17, no. 2, pp. 215–220, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Boyerinas, S.-M. Park, A. Hau, A. E. Murmann, and M. E. Peter, “The role of let-7 in cell differentiation and cancer,” Endocrine-Related Cancer, vol. 17, no. 1, pp. F19–F36, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. A. C. Mueller, D. Sun, and A. Dutta, “The miR-99 family regulates the DNA damage response through its target SNF2H,” Oncogene, vol. 32, no. 9, pp. 1164–1172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Sun, Y. S. Lee, A. Malhotra et al., “miR-99 family of microRNAs suppresses the expression of prostate-specific antigen and prostate cancer cell proliferation,” Cancer Research, vol. 71, no. 4, pp. 1313–1324, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Ozen, C. J. Creighton, M. Ozdemir, and M. Ittmann, “Widespread deregulation of microRNA expression in human prostate cancer,” Oncogene, vol. 27, no. 12, pp. 1788–1793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. E. S. Martens-Uzunova, S. E. Jalava, N. F. Dits et al., “Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer,” Oncogene, vol. 31, no. 8, pp. 978–991, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. O. Larne, E. Martens-Uzunova, Z. Hagman et al., “MiQ—a novel microRNA based diagnostic and prognostic tool for prostate cancer,” International Journal of Cancer, vol. 132, no. 12, pp. 2867–2875, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Moltzahn, A. B. Olshen, L. Baehner et al., “Microfluidic-based multiplex qRT-PCR identifies diagnostic and prognostic microRNA signatures in the sera of prostate cancer patients,” Cancer Research, vol. 71, no. 2, pp. 550–560, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. M. R. Cooperberg, J. M. Broering, and P. R. Carroll, “Risk assessment for prostate cancer metastasis and mortality at the time of diagnosis,” Journal of the National Cancer Institute, vol. 101, no. 12, pp. 878–887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. R. J. Bryant, T. Pawlowski, J. W. F. Catto et al., “Changes in circulating microRNA levels associated with prostate cancer,” British Journal of Cancer, vol. 106, no. 4, pp. 768–774, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Srivastava, H. Goldberger, A. Dimtchev et al., “MicroRNA profiling in prostate cancer—the diagnostic potential of urinary miR-205 and miR-214,” Plos One, vol. 8, no. 10, Article ID e76994, 2013. View at Publisher · View at Google Scholar
  50. T. A. Haj-Ahmad, M. A. K. Abdalla, and Y. Haj-Ahmad, “Potential urinary miRNA biomarker candidates for the accurate detection of prostate cancer among benign prostatic hyperplasia patients,” Journal of Cancer, vol. 5, no. 3, pp. 182–191, 2014. View at Google Scholar
  51. J. Li, P. Smyth, R. Flavin et al., “Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells,” BMC Biotechnology, vol. 7, article 36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. A. J. Stephenson, M. W. Kattan, J. A. Eastham et al., “Defining biochemical recurrence of prostate cancer after radical prostatectomy: a proposal for a standardized definition,” Journal of Clinical Oncology, vol. 24, no. 24, pp. 3973–3978, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. A. W. Tong, P. Fulgham, C. Jay et al., “MicroRNA profile analysis of human prostate cancers,” Cancer Gene Therapy, vol. 16, no. 3, pp. 206–216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Schaefer, M. Jung, H.-J. Mollenkopf et al., “Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma,” International Journal of Cancer, vol. 126, no. 5, pp. 1166–1176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Hulf, T. Sibbritt, E. D. Wiklund et al., “Epigenetic-induced repression of microRNA-205 is associated with MED1 activation and a poorer prognosis in localized prostate cancer,” Oncogene, vol. 32, no. 23, pp. 2891–2899, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Chen, C. Zhang, D. Wu et al., “Phospho-MED1-enhanced UBE2C locus looping drives castration-resistant prostate cancer growth,” The EMBO Journal, vol. 30, no. 12, pp. 2405–2419, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. Z. Hagman, B. S. Haflidadóttir, J. A. Ceder et al., “MiR-205 negatively regulates the androgen receptor and is associated with adverse outcome of prostate cancer patients,” British Journal of Cancer, vol. 108, no. 8, pp. 1668–1676, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Boll, K. Reiche, K. Kasack et al., “MiR-130a, miR-203 and miR-205 jointly repress key oncogenic pathways and are downregulated in prostate carcinoma,” Oncogene, vol. 32, no. 3, pp. 277–285, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Wang, Q. Li, N. H. Feng et al., “miR-205 is frequently downregulated in prostate cancer and acts as a tumor suppressor by inhibiting tumor growth,” Asian Journal of Andrology, vol. 15, no. 6, pp. 735–741, 2013. View at Google Scholar
  60. B. Verdoodt, M. Neid, M. Vogt et al., “MicroRNA-205, a novel regulator of the anti-apoptotic protein Bcl2, is downregulated in prostate cancer,” International Journal of Oncology, vol. 43, no. 1, pp. 307–314, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Mittal, D. Chitkara, S. W. Behrman, and R. Mahato, “Efficacy of gemcitabine conjugated and miRNA-205 complexed micelles for treatment of advanced pancreatic cancer,” Biomaterials, vol. 35, no. 25, pp. 7077–7087, 2014. View at Google Scholar
  62. M. Schubert, M. Spahn, S. Kneitz et al., “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, vol. 8, no. 6, Article ID e65064, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Nadiminty, R. Tummala, W. Lou et al., “MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of myc expression in prostate cancer cells,” The Journal of Biological Chemistry, vol. 287, no. 2, pp. 1527–1537, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. C. A. Gebeshuber and J. Martinez, “MiR-100 suppresses IGF2 and inhibits breast tumorigenesis by interfering with proliferation and survival signaling,” Oncogene, vol. 32, no. 27, pp. 3306–3310, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Xu, Q. Zeng, W. Xu et al., “miRNA-100 inhibits human bladder urothelial carcinogenesis by directly targeting mTOR,” Molecular Cancer Therapeutics, vol. 12, no. 2, pp. 207–219, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. K. R. M. Leite, A. Tomiyama, S. T. Reis et al., “MicroRNA-100 expression is independently related to biochemical recurrence of prostate cancer,” Journal of Urology, vol. 185, no. 3, pp. 1118–1122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Garofalo, C. Quintavalle, G. Romano, C. M. Croce, and G. Condorelli, “miR221/222 in cancer: their role in tumor progression and response to therapy,” Current Molecular Medicine, vol. 12, no. 1, pp. 27–33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Galardi, N. Mercatelli, E. Giorda et al., “miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1,” The Journal of Biological Chemistry, vol. 282, no. 32, pp. 23716–23724, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Fornari, L. Gramantieri, M. Ferracin et al., “MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma,” Oncogene, vol. 27, no. 43, pp. 5651–5661, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Sun, Q. Wang, S. Balk, M. Brown, G.-S. M. Lee, and P. Kantoff, “The role of microrna-221 and microrna-222 in Androgen- independent prostate cancer cell lines,” Cancer Research, vol. 69, no. 8, pp. 3356–3363, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Spahn, S. Kneitz, C.-J. Scholz et al., “Expression of microRNA-221 is progressively reduced in aggressive prostate cancer and metastasis and predicts clinical recurrence,” International Journal of Cancer, vol. 127, no. 2, pp. 394–403, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. O. F. Karatas, E. Guzel, I. Suer et al., “miR-1 and miR-133b are differentially expressed in patients with recurrent prostate cancer,” PloS ONE, vol. 9, p. 6, 2014. View at Google Scholar
  73. M. B. Stope, A. Behr, B. Limbäcker, and C. Krüger, “Heat-shock protein HSPB1 attenuates microRNA miR-1 expression thereby restoring oncogenic pathways in prostate cancer cells,” Anticancer Research, vol. 34, no. 7, pp. 3475–3480, 2014. View at Google Scholar
  74. W. Mo, J. Zhang, X. Li et al., “Identification of novel AR-targeted microRNAs mediating androgen signalling through critical pathways to regulate cell viability in prostate cancer,” PLoS ONE, vol. 8, no. 2, Article ID e56592, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. X. Li, C. Lee, P. Joseph, and et al, “Identification of miR-133b and RB1CC1 as independent predictors for biochemical recurrence and potential therapeutic targets for prostate cancer,” Clinical Cancer Research, vol. 20, no. 9, pp. 2312–2325, 2014. View at Google Scholar
  76. C. Huggins and C. V. Hodges, “Studies on prostatic cancer. I: the effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate,” Journal of Urology, vol. 167, part 2, no. 2, pp. 948–952, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. A. M. Krichevsky and G. Gabriely, “miR-21: a small multi-faceted RNA,” Journal of Cellular and Molecular Medicine, vol. 13, no. 1, pp. 39–53, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. I. A. Asangani, S. A. K. Rasheed, D. A. Nikolova et al., “MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer,” Oncogene, vol. 27, no. 15, pp. 2128–2136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. L. B. Frankel, N. R. Christoffersen, A. Jacobsen, M. Lindow, A. Krogh, and A. H. Lund, “Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells,” The Journal of Biological Chemistry, vol. 283, no. 2, pp. 1026–1033, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Meng, R. Henson, H. Wehbe-Janek, K. Ghoshal, S. T. Jacob, and T. Patel, “MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer,” Gastroenterology, vol. 133, no. 2, pp. 647–658, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. S. Zhu, M.-L. Si, H. Wu, and Y.-Y. Mo, “MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1),” The Journal of Biological Chemistry, vol. 282, no. 19, pp. 14328–14336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. D. Sayed, S. Rane, J. Lypowy et al., “MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths,” Molecular Biology of the Cell, vol. 19, no. 8, pp. 3272–3282, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Gabriely, T. Wurdinger, S. Kesari et al., “MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators,” Molecular and Cellular Biology, vol. 28, no. 17, pp. 5369–5380, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. T. Li, R.-S. Li, Y.-H. Li et al., “MiR-21 as an independent biochemical recurrence predictor and potential therapeutic target for prostate cancer,” The Journal of Urology, vol. 187, no. 4, pp. 1466–1472, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Ribas, X. Ni, M. Haffner et al., “miR-21: an androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth,” Cancer Research, vol. 69, no. 18, pp. 7165–7169, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. A. V. D'Amico, R. Whittington, S. B. Malkowicz et al., “Biochemical outcome after radical prostatectomy or external beam radiation therapy for patients with clinically localized prostate carcinoma in the prostate specific antigen era,” Cancer, vol. 95, no. 2, pp. 281–286, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Shen, G. W. Hruby, J. M. McKiernan et al., “Dysregulation of circulating microRNAs and prediction of aggressive prostate cancer,” Prostate, vol. 72, no. 13, pp. 1469–1477, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. H.-L. Zhang, L.-F. Yang, Y. Zhu et al., “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, vol. 71, no. 3, pp. 326–331, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. V. Coppola, M. Musumeci, M. Patrizii et al., “BTG2 loss and miR-21 upregulation contribute to prostate cell transformation by inducing luminal markers expression and epithelial-mesenchymal transition,” Oncogene, vol. 32, no. 14, pp. 1843–1853, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. S. E. Jalava, A. Urbanucci, L. Latonen et al., “Androgen-regulated miR-32 targets BTG2 and is overexpressed in castration-resistant prostate cancer,” Oncogene, vol. 31, no. 41, pp. 4460–4471, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. C.-J. Kao, A. Martiniez, X.-B. Shi et al., “miR-30 as a tumor suppressor connects EGF/Src signal to ERG and EMT,” Oncogene, vol. 33, no. 19, pp. 2495–24503, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. P. A. Gregory, A. G. Bert, E. L. Paterson et al., “The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1,” Nature Cell Biology, vol. 10, no. 5, pp. 593–601, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. P. Gandellini, E. Giannoni, A. Casamichele et al., “miR-205 hinders the malignant interplay between prostate cancer cells and associated fibroblasts,” Antioxidants & Redox Signaling, vol. 20, no. 7, pp. 1045–1059, 2014. View at Google Scholar
  94. X. Peng, W. Guo, T. Liu et al., “Identification of miRs-143 and -145 that is associated with bone metastasis of prostate cancer and involved in the regulation of EMT,” PLoS ONE, vol. 6, no. 5, Article ID e20341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Saini, S. Majid, S. Yamamura et al., “Regulatory role of mir-203 in prostate cancer progression and metastasis,” Clinical Cancer Research, vol. 17, no. 16, pp. 5287–5298, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. X. Yu, X. Jiang, H. Li, L. Guo, and S. H. Lu, “miR-203 inhibits the proliferation and self-renewal of esophageal cancer stem-like cells by suppressing stem renewal factor Bmi-1,” Stem Cells and Development, vol. 23, no. 6, pp. 576–585, 2014. View at Google Scholar
  97. D. Bonci, V. Coppola, M. Musumeci et al., “The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities,” Nature Medicine, vol. 14, no. 11, pp. 1271–1277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Musumeci, V. Coppola, A. Addario et al., “Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer,” Oncogene, vol. 30, no. 41, pp. 4231–4242, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. F. Takeshita, L. Patrawala, M. Osaki et al., “Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes,” Molecular Therapy, vol. 18, no. 1, pp. 181–187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. J. C. Brase, M. Johannes, T. Schlomm et al., “Circulating miRNAs are correlated with tumor progression in prostate cancer,” International Journal of Cancer, vol. 128, no. 3, pp. 608–616, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. H.-L. Zhang, X.-J. Qin, D.-L. Cao et al., “An elevated serum miR-141 level in patients with bone-metastatic prostate cancer is correlated with more bone lesions,” Asian Journal of Andrology, vol. 15, no. 2, pp. 231–235, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. L. A. Selth, S. L. Townley, A. G. Bert et al., “Circulating microRNAs predict biochemical recurrence in prostate cancer patients,” British Journal of Cancer, vol. 109, no. 3, pp. 641–650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. H. C. Nguyen, W. Xie, M. Yang et al., “Expression differences of circulating microRNAs in metastatic castration resistant prostate cancer and low-risk, localized prostate cancer,” Prostate, vol. 73, no. 4, pp. 346–354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. C. Parker, S. Nilsson, D. Heinrich et al., “Alpha emitter radium-223 and survival in metastatic prostate cancer,” The New England Journal of Medicine, vol. 369, no. 3, pp. 213–223, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. R. P. Smith, D. E. Heron, M. S. Huq, and N. J. Yue, “Modern radiation treatment planning and delivery—from Rontgen to real time,” Hematology/Oncology Clinics of North America, vol. 20, no. 1, pp. 45–62, 2006. View at Google Scholar
  106. S. A. Bhide and C. M. Nutting, “Recent advances in radiotherapy,” BMC Medicine, vol. 8, article 25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. S. Josson, S.-Y. Sung, K. Lao, L. W. K. Chung, and P. A. S. Johnstone, “Radiation modulation of microRNA in prostate cancer cell lines,” Prostate, vol. 68, no. 15, pp. 1599–1606, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Li, X.-B. Shi, D. Nori et al., “Down-regulation of microRNA 106b is involved in p21-mediated cell cycle arrest in response to radiation in prostate cancer cells,” Prostate, vol. 71, no. 6, pp. 567–574, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. I. Ivanovska, A. S. Ball, R. L. Diaz et al., “MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression,” Molecular and Cellular Biology, vol. 28, no. 7, pp. 2167–2174, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. X. Huang, S. Taeb, S. Jahangiri et al., “miRNA-95 mediates radioresistance in tumors by targeting the sphingolipid phosphatase SGPP1,” Cancer Research, vol. 73, no. 23, pp. 6972–6986, 2013. View at Google Scholar
  111. M. R. Epis, K. M. Giles, A. Barker, T. S. Kendrick, and P. J. Leedman, “miR-331-3p regulates ERBB-2 expression and androgen receptor signaling in prostate cancer,” The Journal of Biological Chemistry, vol. 284, no. 37, pp. 24696–24704, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. S. Isharwal, M. C. Miller, J. I. Epstein et al., “Prognostic value of Her-2/neu and DNA index for progression, metastasis and prostate cancer-specific death in men with long-term follow-up after radical prostatectomy,” International Journal of Cancer, vol. 123, no. 11, pp. 2636–2643, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Ottman, C. Nguyen, R. Lorch, and R. Chakrabarti, “MicroRNA expressions associated with progression of prostate cancer cells to antiandrogen therapy resistance,” Molecular Cancer, vol. 13, article 1, 2014. View at Publisher · View at Google Scholar
  114. S. Lehmusvaara, T. Erkkilä, A. Urbanucci et al., “Goserelin and bicalutamide treatments alter the expression of microRNAs in the prostate,” Prostate, vol. 73, no. 1, pp. 101–112, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. K. McKeage, “Docetaxel: a review of its use for the first-line treatment of advanced castration-resistant prostate cancer,” Drugs, vol. 72, no. 11, pp. 1559–1577, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Puhr, J. Hoefer, G. Schäfer et al., “Epithelial-to-mesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205,” The American Journal of Pathology, vol. 181, no. 6, pp. 2188–2201, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Pennati, A. Lopergolo, V. Profumo et al., “miR-205 impairs the autophagic flux and enhances cisplatin cytotoxicity in castration-resistant prostate cancer cells,” Biochemical Pharmacology, vol. 87, no. 4, pp. 579–597, 2014. View at Publisher · View at Google Scholar
  118. H. M. Lin, L. Castillo, K. L. Mahon et al., “Circulating microRNAs are associated with docetaxel chemotherapy outcome in castration-resistant prostate cancer,” British Journal of Cancer, vol. 110, no. 10, pp. 2462–2471, 2014. View at Google Scholar
  119. K. Kojima, Y. Fujita, Y. Nozawa, T. Deguchi, and M. Ito, “MiR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms,” Prostate, vol. 70, no. 14, pp. 1501–1512, 2010. View at Publisher · View at Google Scholar · View at Scopus
  120. O. W. Rokhlin, V. S. Scheinker, A. F. Taghiyev, D. Bumcrot, R. A. Glover, and M. B. Cohen, “MicroRNA-34 mediates AR-dependent p53-induced apoptosis in prostate cancer,” Cancer Biology & Therapy, vol. 7, no. 8, pp. 1288–1296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. Y. Fujita, K. Kojima, R. Ohhashi et al., “MiR-148a attenuates paclitaxel resistance of hormone-refractory, drug-resistant prostate cancer PC3 cells by regulating MSK1 expression,” The Journal of Biological Chemistry, vol. 285, no. 25, pp. 19076–19084, 2010. View at Publisher · View at Google Scholar · View at Scopus
  122. D. Kong, S. Banerjee, A. Ahmad et al., “Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells,” PLoS ONE, vol. 5, no. 8, Article ID e12445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. M. Maugeri-Sacca, A. Zeuner, and R. De Maria, “Therapeutic targeting of cancer stem cells,” Frontiers in Oncology, vol. 1, p. 17, 2011. View at Google Scholar
  124. A. Zeuner and R. De Maria, “Not so lonely at the top for cancer stem cells,” Cell Stem Cell, vol. 9, no. 4, pp. 289–290, 2011. View at Publisher · View at Google Scholar · View at Scopus
  125. C. Liu, K. Kelnar, A. V. Vlassov, D. Brown, J. Wang, and D. G. Tang, “Distinct microRNA expression profiles in prostate cancer stem/progenitor cells and tumor-suppressive functions of let-7,” Cancer Research, vol. 72, no. 13, pp. 3393–3404, 2012. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Saini, S. Majid, V. Shahryari et al., “miRNA-708 control of CD44+ prostate cancer-initiating cells,” Cancer Research, vol. 72, no. 14, pp. 3618–3630, 2012. View at Publisher · View at Google Scholar · View at Scopus
  127. S. Huang, W. Guo, Y. Tang, D. Ren, X. Zou, and X. Peng, “miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells,” Oncology Reports, vol. 28, no. 5, pp. 1831–1837, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. X. Fan, X. Chen, W. Deng, G. Zhong, Q. Cai, and T. Lin, “Up-regulated microRNA-143 in cancer stem cells differentiation promotes prostate cancer cells metastasis by modulating FNDC3B expression,” BMC Cancer, vol. 13, article 61, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. I.-S. Hsieh, K.-C. Chang, Y.-T. Tsai et al., “MicroRNA-320 suppresses the stem cell-like characteristics of prostate cancer cells by downregulating the Wnt/beta-catenin signaling pathway,” Carcinogenesis, vol. 34, no. 3, pp. 530–538, 2013. View at Publisher · View at Google Scholar · View at Scopus
  130. A. G. Bader, D. Brown, J. Stoudemire, and P. Lammers, “Developing therapeutic microRNAs for cancer,” Gene Therapy, vol. 18, no. 12, pp. 1121–1126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  131. E. van Rooij, A. L. Purcell, and A. A. Levin, “Developing MicroRNA therapeutics,” Circulation Research, vol. 110, no. 3, pp. 496–507, 2012. View at Publisher · View at Google Scholar · View at Scopus
  132. F. Qu, X. Cui, Y. Hong et al., “MicroRNA-185 suppresses proliferation, invasion, migration, and tumorigenicity of human prostate cancer cells through targeting androgen receptor,” Molecular and Cellular Biochemistry, vol. 377, no. 1-2, pp. 121–130, 2013. View at Publisher · View at Google Scholar · View at Scopus
  133. P. C. Lin, Y. L. Chiu, S. Banerjee et al., “Epigenetic repression of miR-31 disrupts androgen receptor homeostasis and contributes to prostate cancer progression,” Cancer Research, vol. 73, no. 3, pp. 1232–1244, 2013. View at Publisher · View at Google Scholar · View at Scopus
  134. K. Sikand, J. E. Slaibi, R. Singh, S. D. Slane, and G. C. Shukla, “miR 488* inhibits androgen receptor expression in prostate carcinoma cells,” International Journal of Cancer, vol. 129, no. 4, pp. 810–819, 2011. View at Publisher · View at Google Scholar · View at Scopus
  135. P. Östling, S.-K. Leivonen, A. Aakula et al., “Systematic analysis of microRNAs targeting the androgen receptor in prostate cancer cells,” Cancer Research, vol. 71, no. 5, pp. 1956–1967, 2011. View at Publisher · View at Google Scholar · View at Scopus