Early Detections and Diagnosis

You have full text access to this OnlineOpen article

Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma

  1. Annika Schaefer1,2,3,†,
  2. Monika Jung2,†,
  3. Hans-Joachim Mollenkopf4,
  4. Ina Wagner4,
  5. Carsten Stephan2,
  6. Florian Jentzmik2,
  7. Kurt Miller2,
  8. Michael Lein2,3,
  9. Glen Kristiansen5,†,
  10. Klaus Jung2,3,†,‡,*

Article first published online: 12 AUG 2009

DOI: 10.1002/ijc.24827

Issue

International Journal of Cancer

International Journal of Cancer

Volume 126, Issue 5, pages 1166–1176, 1 March 2010

Additional Information

How to Cite

Schaefer, A., Jung, M., Mollenkopf, H.-J., Wagner, I., Stephan, C., Jentzmik, F., Miller, K., Lein, M., Kristiansen, G. and Jung, K. (2010), Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int. J. Cancer, 126: 1166–1176. doi: 10.1002/ijc.24827

Author Information

  1. 1

    Department of Biology, Chemistry and Pharmacy, Free University, Berlin, Germany

  2. 2

    Department of Urology, University Hospital Charité, Berlin, Germany

  3. 3

    Berlin Institute for Urologic Research, Berlin, Germany

  4. 4

    Max Planck Institute for Infection Biology, Berlin, Germany

  5. 5

    Department of Surgical Pathology, University Hospital Zurich, Zurich, Switzerland

  1. †

    Annika Schaefer, Monika Jung, Glen Kristiansen and Klaus Jung contributed equally to this work

  2. ‡

    Fax: +4930450515904

*Department of Urology, University Hospital Charité, Schumannstr. 20/21, Berlin 10117, Germany

Publication History

  1. Issue published online: 27 DEC 2009
  2. Article first published online: 12 AUG 2009
  3. Accepted manuscript online: 12 AUG 2009 12:00AM EST
  4. Manuscript Accepted: 4 AUG 2009
  5. Manuscript Received: 24 APR 2009

Funded by

  • Urologic Research Foundation Berlin, SONNENFELD Foundation

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (473K)

References

  • 1
    Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9: 102–14.
  • 2
    Berezikov E, Guryev V, van de Belt J, Wienholds E, Plasterk RH, Cuppen E. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005; 120: 21–4.
  • 3
    Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99: 15524–9.
  • 4
    Roldo C, Missiaglia E, Hagan JP, Falconi M, Capelli P, Bersani S, Calin GA, Volinia S, Liu CG, Scarpa A, Croce CM. MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 2006; 24: 4677–84.
  • 5
    Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005; 65: 7065–70.
  • 6
    Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, Calin GA, Menard S, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007; 67: 8699–707.
  • 7
    Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA,Jr, Sjoblom T, Barad O, Bentwich Z, Szafranska AE, Labourier E, Raymond CK, Roberts BS, et al. The colorectal microRNAome. Proc Natl Acad Sci USA 2006; 103: 3687–92.
  • 8
    Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189–98.
  • 9
    Molnar V, Tamasi V, Bakos B, Wiener Z, Falus A. Changes in miRNA expression in solid tumors: an miRNA profiling in melanomas. Semin Cancer Biol 2008; 18: 111–22.
  • 10
    Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DL, Au GK, Liu CG, Calin GA, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008; 299: 425–36.
  • 11
    Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, et al. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 2008; 68: 6162–70.
  • 12
    Ozen M, Creighton CJ, Ozdemir M, Ittmann M. Widespread deregulation of microRNA expression in human prostate cancer. Oncogene 2008; 27: 1788–93.
  • 13
    Porkka KP, Pfeiffer MJ, Waltering KK, Vessella RL, Tammela TL, Visakorpi T. MicroRNA expression profiling in prostate cancer. Cancer Res 2007; 67: 6130–5.
  • 14
    Tong AW, Fulgham P, Jay C, Chen P, Khalil I, Liu S, Senzer N, Eklund AC, Han J, Nemunaitis J. MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther 2009; 16: 206–16.
  • 15
    Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257–61.
  • 16
    Schaefer A, Jung M, Kristiansen G, Lein M, Schrader M, Miller K, Stephan C, Jung K. MicroRNAs and cancer: current state and future perspectives in urologic oncology. Urol Oncol, [Epub ahead of print], December 29, 2008; doi:10.1016/j.urolonc.2008.10.021.
  • 17
    Lin SL, Chiang A, Chang D, Ying SY. Loss of mir-146a function in hormone-refractory prostate cancer. RNA 2008; 14: 417–24.
  • 18
    Sobin LH, Wittekind C. TNM classification of malignant tumours, 6 edn. New York: Wiley-Liss, 2002. 184–7.
  • 19
    Epstein JI, Allsbrook WC,Jr, Amin MB, Egevad LL. The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on gleason grading of prostatic carcinoma. Am J Surg Pathol 2005; 29: 1228–42.
  • 20
    Jung M, Mollenkopf H-J, Grimm C, Wagner I, Albrecht M, Waller T, Pilarsky C, Johannsen M, Stephan C, Lehrach H, Nietfeld W, Rudel T, et al. MicroRNA profiling of clear cell renal cell cancer identifies a robust signature to define renal malignancy. J Cell Mol Med, [Epub ahead of print], February 17, 2009; doi: 10.1111/j.1582-4934.2009. 00705.x.
  • 21
    Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonak J, Lind K, Sindelka R, Sjoback R, Sjogreen B, Strombom L, Stahlberg A, Zoric N. The real-time polymerase chain reaction. Mol Aspects Med 2006; 27: 95–125.
  • 22
    Schröder B. Evaluating the predictive performance of species distribution models. 2006. Available at: http://brandenburg.geoecology. uni-potsdam.de/users/schroeder/download.html. Accessed 21 June 2009.
  • 23
    Guillonneau B, el-Fettouh H, Baumert H, Cathelineau X, Doublet JD, Fromont G, Vallancien G. Laparoscopic radical prostatectomy: oncological evaluation after 1,000 cases a Montsouris Institute. J Urol 2003; 169: 1261–6.
  • 24
    Lein M, Stibane I, Mansour R, Hege C, Roigas J, Wille A, Jung K, Kristiansen G, Schnorr D, Loening SA, Deger S. Complications, urinary continence, and oncologic outcome of 1000 laparoscopic transperitoneal radical prostatectomies-experience at the Charite Hospital Berlin Campus Mitte. Eur Urol 2006; 50: 1278–82.
  • 25
    Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan DA, Li A, Huang G, Klein-Szanto AJ, Gimotty PA, Katsaros D, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 2008; 10: 202–10.
  • 26
    Yang K, Handorean AM, Iczkowski KA. MicroRNAs 373 and 520c are downregulated in prostate cancer, suppress CD44 translation and enhance invasion of prostate cancer cells in vitro. Int J Clin Exp Pathol 2009; 2: 361–9.
  • 27
    Haller F, Kulle B, Schwager S, Gunawan B, von HA, Sultmann H, Fuzesi L. Equivalence test in quantitative reverse transcription polymerase chain reaction: confirmation of reference genes suitable for normalization. Anal Biochem 2004; 335: 1–9.
  • 28
    Harrell FE,Jr. Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. New York: Springer-Verlag, 2001. 247–9.
  • 29
    Kleinbaum DG. Survival analysis: a self-learning text. New York: Springer-Verlag, 1996. 129–50.
  • 30
    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, et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008; 14: 1271–7.
  • 31
    Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102: 13944–9.
  • 32
    Guo J, Miao Y, Xiao B, Huan R, Jiang Z, Meng D, Wang Y. Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J Gastroenterol Hepatol 2009; 24: 652–7.
  • 33
    Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM, Farace MG. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 2005; 334: 1351–8.
  • 34
    Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, Ju J, Kornmann M, Ju J. Prognostic values of microRNAs in colorectal cancer. Biomark Insights 2006; 2: 113–21.
  • 35
    Wong TS, Liu XB, Wong BY, Ng RW, Yuen AP, Wei WI. Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin Cancer Res 2008; 14: 2588–92.
  • 36
    Chen Y, Stallings RL. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Res 2007; 67: 976–83.
  • 37
    Xu S, Witmer PD, Lumayag S, Kovacs B, Valle D. MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J Biol Chem 2007; 282: 25053–66.
  • 38
    Agirre X, Jimenez-Velasco A, San Jose-Eneriz E, Garate L, Bandres E, Cordeu L, Aparicio O, Saez B, Navarro G, Vilas-Zornoza A, Perez-Roger I, Garcia-Foncillas J, et al. Down-regulation of hsa-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth. Mol Cancer Res 2008; 6: 1830–40.
  • 39
    Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, Zucman-Rossi J. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 2008; 47: 1955–63.
  • 40
    Lu J, Getz G, Miska EA, varez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834–8.
  • 41
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105: 10513–18.
  • 42
    Hessels D, Klein Gunnewiek JM, van OI, Karthaus HF, van Leenders GJ, van BB, Kiemeney LA, Witjes JA, Schalken JA. DD3(PCA3)-based molecular urine analysis for the diagnosis of prostate cancer. Eur Urol 2003; 44: 8–15.
  • 43
    Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, Vere White RW. An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci USA 2007; 104: 19983–8.
  • 44
    Lee YS, Kim HK, Chung S, Kim KS, Dutta A. Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. J Biol Chem 2005; 280: 16635–41.
  • 45
    Mercatelli N, Coppola V, Bonci D, Miele F, Costantini A, Guadagnoli M, Bonanno E, Muto G, Frajese GV, De MR, Spagnoli LG, Farace MG, et al. The inhibition of the highly expressed miR-221 and miR-222 impairs the growth of prostate carcinoma xenografts in mice. PLoS ONE 2008; 3: e4029.
  • 46
    Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafre SA, Farace MG. miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 2007; 282: 23716–24.
  • 47
    Kim SW, Hayashi M, Lo JF, Yang Y, Yoo JS, Lee JD. ADP-ribosylation factor 4 small GTPase mediates epidermal growth factor receptor-dependent phospholipase D2 activation. J Biol Chem 2003; 278: 2661–8.
  • 48
    Childs G, Fazzari M, Kung G, Kawachi N, Brandwein-Gensler M, McLemore M, Chen Q, Burk RD, Smith RV, Prystowsky MB, Belbin TJ, Schlecht NF. Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am J Pathol 2009; 174: 736–45.
  • 49
    Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, Wells W, Kauppinen S, Cole CN. Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 2007; 67: 11612–20.
  • 50
    Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593–601.
  • 51
    Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC. Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 2008; 183: 143–55.
  • 52
    McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 2005; 97: 1180–4.
View Full Article with Supporting Information (HTML) Get PDF (473K)