Loss of PTEN is associated with aggressive behavior in ERG-positive prostate cancer

Cancer Epidemiology Biomarkers and Prevention

Volumn 22, Issue 12, 2013, Pages 2333-2344

  Leinonen, Katri A ^a   Saramäki, Outi R ^a   Furusato, Bungo ^b   Kimura, Takahiro ^b   Takahashi, Hiroyuki ^b   Egawa, Shin ^b   Suzuki, Hiroyoshi ^c   Keiger, Kerri ^d   Hahm, Sung Ho ^d   Isaacs, William B ^d   Tolonen, Teemu T ^a   Stenman, Ulf Håkan ^e   Tammela, Teuvo L J ^a   Nykter, Matti ^a   Bova, G Steven ^a   Visakorpi, Tapio ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TOHO UNIVERSITY SAKURA MEDICAL CENTER   (Japan)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; PROTEIN P53; TRANSCRIPTION FACTOR ERG; TRANSMEMBRANE PROTEASE SERINE 2; TUMOR PROTEIN; UNCLASSIFIED DRUG;

AGGRESSION; ARTICLE; CANCER HORMONE THERAPY; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SURGERY; CANCER SURVIVAL; CASTRATION RESISTANT PROSTATE CANCER; COHORT ANALYSIS; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FUSION; GENE LOSS; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LOCAL METASTASIS; MAJOR CLINICAL STUDY; MALE; NEEDLE BIOPSY; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATECTOMY; PROTEIN PROTEIN INTERACTION; PTEN GENE; TRANSURETHRAL RESECTION; TUMOR BIOPSY; TUMOR GENE;

COHORT STUDIES; DISEASE-FREE SURVIVAL; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; NEOPLASM METASTASIS; ONCOGENE PROTEINS, FUSION; PARAFFIN EMBEDDING; PROSTATECTOMY; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; PTEN PHOSPHOHYDROLASE; SERINE ENDOPEPTIDASES; TRANS-ACTIVATORS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84890061009     PISSN: 10559965     EISSN: None     Source Type: Journal    
DOI: 10.1158/1055-9965.EPI-13-0333-T     Document Type: Article

References (48)

1. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. Recurrent gene fusions in prostate cancer. Nat Rev Cancer 2008;8:497-511.
2. Lin B, Ferguson C, White JT, Wang S, Vessella R, True LD, et al. Prostate-localized and androgen-regulated expression of the membrane-bound serine protease TMPRSS2. Cancer Res 1999;59: 4180-4.
3. Afar DE, Vivanco I, Hubert RS, Kuo J, Chen E, Saffran DC, et al. Catalytic cleavage of the androgen-regulated TMPRSS2 protease results in its secretion by prostate and prostate cancer epithelia. Cancer Res 2001;61:1686-92.
4. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310:644-8.
5. Pflueger D, Rickman DS, Sboner A, Perner S, LaFargue CJ, Svensson MA, et al. N-myc downstream regulated gene 1 (NDRG1) is fused to ERG in prostate cancer. Neoplasia 2009;11:804-11.
6. Saramäki OR, Harjula AE, Martikainen PM, Vessella RL, Tammela TL, Visakorpi T. TMPRSS2:ERG fusion identifies a subgroup of prostate cancers with a favorable prognosis. Clin Cancer Res 2008; 14:3395-400.
7. Petrovics G, Liu A, Shaheduzzaman S, Furusato B, Sun C, Chen Y, et al. Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene 2005;24:3847-52.
8. Wang J, Cai Y, Ren C, Ittmann M. Expression of variant TMPRSS/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res 2006;66:8347-51.
9. Demichelis F, Fall K, Perner S, Andrén O, Schmidt F, Setlur SR, et al. TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene 2007;26:4596-9.
10. Nam RK, Sugar L, Yang W, Srivastava S, Klotz LH, Yang LY, et al. Expression of the TMPRSS2:ERG fusion gene predicts cancer recurrence after surgery for localised prostate cancer. Br J Cancer 2007; 97:1690-5.
11. Lapointe J, Kim YH, Miller MA, Li C, Kaygusuz G, van de Rijn M, et al. A variant TMPRSS2 isoform and ERG fusion product in prostate cancer with implications for molecular diagnosis. Mod Pathol 2007;20: 467-73.
12. Gopalan A, Leversha MA, Satagopan JM, Zhou Q, Al-Ahmadie HA, Fine SW, et al. TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy. Cancer Res 2009; 69:1400-6.
13. Pettersson A, Graff RE, Bauer SR, Pitt MJ, Lis RT, Stack EC, et al. The TMPRSS2:ERG Rearrangement, ERG Expression, and Prostate Cancer Outcomes: A Cohort Study and Meta-analysis. Cancer Epidemiol Biomarkers Prev 2012;21:1497-509.
14. Leinonen KA, Tolonen TT, Bracken H, Stenman UH, Tammela TL, Saramäki OR, et al. Association of SPINK1 expression and TMPRSS2: ERG fusion with prognosis in endocrine-treated prostate cancer. Clin Cancer Res 2010;16:2845-51.
15. Boormans JL, Hermans KG, Made AC, van Leenders GJ, Wildhagen MF, Collette L, et al. Expression of the androgen-regulated fusion gene TMPRSS2-ERG does not predict response to endocrine treatment in hormone-naïve, node-positive prostate cancer. Eur Urol 2010;57: 830-5.
16. Li Y, Kong D, Wang Z, Ahmad A, Bao B, Padhye S, et al. Inactivation of AR/TMPRSS2-ERG/Wnt signaling networks attenuates the aggressive behavior of prostate cancer cells. Cancer Prev Res (Phila) 2011;4:1495-506.
17. Yu J, Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010;17: 443-54.
18. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.
19. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH, Taylor BS, et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 2009;41: 524-6.
20. Tomlins SA, Rhodes DR, Yu J, Varambally S, Mehra R, Perner S, et al. The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell 2008;13:519-28.
21. Mulholland DJ, Tran LM, Li Y, Cai H, Morim A, Wang S, et al. Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 2011;19:792-804.
22. Carver BS, Chapinski C, Wongvipat J, Hieronymus H, Chen Y, Chandarlapaty S, et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 2011;19:575-86.
23. Sircar K, Yoshimoto M, Monzon FA, Koumakpayi IH, Katz RL, Khanna A, et al. PTEN genomic deletion is associated with p-Akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol 2009;218:505-13.
24. Wang Y, Romigh T, He X, Tan MH, Orloff MS, Silverman RH, et al. Differential regulation of PTEN expression by androgen receptor in prostate and breast cancers. Oncogene 2011;30:4327-38.
25. Osman S, Turpeinen U, Itkonen O, Stenman UH. Optimization of a time-resolved immunofluorometric assay for tumor-associated trypsin inhibitor (TATI) using the streptavidin-biotin system. J Immunol Methods 1993;161:97-106.
26. Isola J, Tuominen V. JPEG2000 Virtual Slide microscope. 2006. Available from: http://jvsmicroscope.uta.fi
27. Isola J, Tuominen V. ImmunoRatio. 2010. Available from: http://jvsmicroscope.uta.fi/immunoratio
28. Tuominen VJ, Ruotoistenmäki S, Viitanen A, Jumppanen M, Isola J. ImmunoRatio: a publicly available web application for quantitative image analysis of estrogen receptor (ER), progesterone receptor (PR), and Ki-67. Breast Cancer Res 2010;12:R56.
29. Liu W, Laitinen S, Khan S, Vihinen M, Kowalski J, Yu G, et al. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat Med 2009;15:559-65.
30. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, Sidransky D, et al. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 1998;58:204-9.
31. Minner S, Enodien M, Sirma H, Luebke AM, Krohn A, Mayer PS, et al. ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy. Clin Cancer Res 2011;17:5878-88.
32. Hoogland AM, Jenster G, van Weerden WM, Trapman J, van der Kwast T, Roobol MJ, et al. ERG immunohistochemistry is not predictive for PSA recurrence, local recurrence or overall survival after radical prostatectomy for prostate cancer. Mod Pathol 2012;25:471-9.
33. Chng KR, Chang CW, Tan SK, Yang C, Hong SZ, Sng NY, et al. A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. EMBO J 2012;31:2810-23.
34. Laitinen S, Martikainen PM, Tolonen T, Isola J, Tammela TL, Visakorpi T. EZH2, Ki-67 and MCM7 are prognostic markers in prostatectomy treated patients. Int J Cancer 2008;122:595-602.
35. Visakorpi T, Hyytinen E, Koivisto P, Tanner M, Keinänen R, Palmberg C, et al. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet 1995;9:401-6.
36. Koivisto P, Kononen J, Palmberg C, Tammela T, Hyytinen E, Isola J, et al. Androgen receptor gene amplification: a possible molecular mechanism for androgen deprivation therapy failure in prostate cancer. Cancer Res 1997;57:314-9.
37. Linja MJ, Savinainen KJ, Saramäki OR, Tammela TL, Vessella RL, Visakorpi T. Amplification and overexpression of androgen receptor gene in hormone-refractory prostate cancer. Cancer Res 2001;61: 3550-5.
38. Yoshimoto M, Cunha IW, Coudry RA, Fonseca FP, Torres CH, Soares FA, et al. FISH analysis of 107 prostate cancers shows that PTEN genomic deletion is associated with poor clinical outcome. Br J Cancer 2007;97:678-85.
39. McCall P, Witton CJ, Grimsley S, Nielsen KV, Edwards J. Is PTEN loss associated with clinical outcome measures in human prostate cancer? Br J Cancer 2008;99:1296-301.
40. McMenamin ME, Soung P, Perera S, Kaplan I, Loda M, Sellers WR. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res 1999;59:4291-6.
41. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 2009;41:619-24.
42. Yoshimoto M, Joshua AM, Cunha IW, Coudry RA, Fonseca FP, Ludkovski O, et al. Absence of TMPRSS2:ERG fusions and PTEN losses in prostate cancer is associated with a favorable outcome. Mod Pathol 2008;21:1451-60.
43. Krohn A, Diedler T, Burkhardt L, Mayer PS, De Silva C, Meyer-Kornblum M, et al. Genomic deletion of PTEN is associated with tumor progression and early PSA recurrence in ERG fusion-positive and fusion-negative prostate cancer. Am J Pathol 2012;181:401-12.
44. Reid AH, Attard G, Ambroisine L, Fisher G, Kovacs G, Brewer D, et al. Molecular characterisation of ERG, ETV1 and PTEN gene loci identifies patients at low and high risk of death from prostate cancer. Br J Cancer 2010;102:678-84.
45. Bookstein R, MacGrogan D, Hilsenbeck SG, Sharkey F, Allred DC. p53 is mutated in a subset of advanced-stage prostate cancers. Cancer Res 1993;53:3369-73.
46. Chi SG, deVere White RW, Meyers FJ, Siders DB, Lee F, Gumerlock PH. p53 in prostate cancer: frequent expressed transition mutations. J Natl Cancer Inst 1994;86:926-33.
47. Shah RB, Mehra R, Chinnaiyan AM, Shen R, Ghosh D, Zhou M, et al. Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program. Cancer Res 2004; 64:9209-16.
48. Park K, Tomlins SA, Mudaliar KM, Chiu YL, Esgueva R, Mehra R, et al. Antibody-based detection of ERG rearrangement-positive prostate cancer. Neoplasia 2010;12:590-8.