The prognostic role of ERG immunopositivity in prostatic acinar adenocarcinoma: A study including 454 cases and review of the literature

Human Pathology

Volumn 45, Issue 3, 2014, Pages 488-497

  Xu, Bin ^a   Chevarie Davis, Myriam ^a   Chevalier, Simone ^a   Scarlata, Eleanora ^a   Zeizafoun, Nebras ^b   Dragomir, Alice ^a   Tanguay, Simon ^a   Kassouf, Wassim ^a   Aprikian, Armen ^a   Brimo, Fadi ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

Author keywords

Biochemical recurrence; ERG; Immunohistochemistry; Prostate adenocarcinoma; TMPRSS2 ERG fusion

Indexed keywords

BIOCHEMICAL RECURRENCE; ERG; IMMUNOHISTOCHEMISTRY; PROSTATE ADENOCARCINOMA; TMPRSS2/ERG FUSION;

CARCINOMA, ACINAR CELL; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; ONCOGENE PROTEINS, FUSION; PROGNOSIS; PROSTATE; PROSTATECTOMY; PROSTATIC NEOPLASMS; TRANS-ACTIVATORS;

EID: 84894104579     PISSN: 00468177     EISSN: 15328392     Source Type: Journal    
DOI: 10.1016/j.humpath.2013.10.012     Document Type: Article

References (86)

1. U.S. Cancer Statitics Working Group. United state cancer statistics: 1999-2009 incidence and mortality Web-based report. 2012. Atlanta, GA: Department of Health and Human Services, Centers for Disease Control and Prevention, and National Cancer Institute.
2. S.A. Tomlins, D.R. Rhodes, and S. Perner et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer Science 310 2005 644 648
3. T.A. Bismar, M. Yoshimoto, and R.T. Vollmer et al. PTEN genomic deletion is an early event associated with ERG gene rearrangements in prostate cancer BJU Int 107 2011 477 485
4. T.A. Bismar, M. Dolph, L.H. Teng, S. Liu, and B. Donnelly ERG protein expression reflects hormonal treatment response and is associated with Gleason score and prostate cancer specific mortality Eur J Cancer 48 2012 538 546
5. M. Braun, V.J. Scheble, and R. Menon et al. Relevance of cohort design for studying the frequency of the ERG rearrangement in prostate cancer Histopathology 58 2011 1028 1036
6. A. Chaux, R. Albadine, and A. Toubaji et al. Immunohistochemistry for ERG expression as a surrogate for TMPRSS2-ERG fusion detection in prostatic adenocarcinomas Am J Surg Pathol 35 2011 1014 1020
7. A.D. Darnel, C.J. Lafargue, R.T. Vollmer, J. Corcos, and T.A. Bismar TMPRSS2-ERG fusion is frequently observed in Gleason pattern 3 prostate cancer in a Canadian cohort Cancer Biol Ther 8 2009 125 130
8. R. Esgueva, S. Perner, and J. LaFargue et al. Prevalence of TMPRSS2-ERG and SLC45A3-ERG gene fusions in a large prostatectomy cohort Mod Pathol 23 2010 539 546
9. S.M. Falzarano, M. Zhou, P. Carver, T. Tsuzuki, K. Simmerman, H. He, and C. Magi-Galluzzi ERG gene rearrangement status in prostate cancer detected by immunohistochemistry Virchows Arch 459 2011 441 447
10. S.M. Falzarano, M. Zhou, A.V. Hernandez, E.A. Klein, M.A. Rubin, and C. Magi-Galluzzi Single focus prostate cancer: pathological features and ERG fusion status J Urol 185 2011 489 494
11. B. Furusato, G.J. van Leenders, and J. Trapman et al. Immunohistochemical ETS-related gene detection in a Japanese prostate cancer cohort: diagnostic use in Japanese prostate cancer patients Pathol Int 61 2011 409 414
12. A. Gopalan, M.A. Leversha, and J.M. Satagopan et al. TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy Cancer Res 69 2009 1400 1406
13. C.C. Guo, G. Zuo, D. Cao, P. Troncoso, and B.A. Czerniak Prostate cancer of transition zone origin lacks TMPRSS2-ERG gene fusion Mod Pathol 22 2009 866 871
14. C.C. Guo, Y. Wang, L. Xiao, P. Troncoso, and B.A. Czerniak The relationship of TMPRSS2-ERG gene fusion between primary and metastatic prostate cancers Hum Pathol 43 2012 644 649
15. A.M. Hoogland, G. Jenster, and W.M. van Weerden et al. ERG immunohistochemistry is not predictive for PSA recurrence, local recurrence or overall survival after radical prostatectomy for prostate cancer Mod Pathol 25 2012 471 479
16. J.M. Mosquera, R. Mehra, and M.M. Regan et al. Prevalence of TMPRSS2-ERG fusion prostate cancer among men undergoing prostate biopsy in the United States Clin Cancer Res 15 2009 4706 4711
17. R.K. Nam, L. Sugar, and W. Yang et al. Expression of the TMPRSS2:ERG fusion gene predicts cancer recurrence after surgery for localised prostate cancer Br J Cancer 97 2007 1690 1695
18. R.K. Nam, L. Sugar, and Z. Wang et al. Expression of TMPRSS2:ERG gene fusion in prostate cancer cells is an important prognostic factor for cancer progression Cancer Biol Ther 6 2007 40 45
19. S. Perner, J.M. Mosquera, and F. Demichelis et al. TMPRSS2-ERG fusion prostate cancer: an early molecular event associated with invasion Am J Surg Pathol 31 2007 882 888
20. O.R. Saramaki, A.E. Harjula, P.M. Martikainen, R.L. Vessella, T.L. Tammela, and T. Visakorpi TMPRSS2:ERG fusion identifies a subgroup of prostate cancers with a favorable prognosis Clin Cancer Res 14 2008 3395 3400
21. V.J. Scheble, M. Braun, and R. Beroukhim et al. ERG rearrangement is specific to prostate cancer and does not occur in any other common tumor Mod Pathol 23 2010 1061 1067
22. G.J. van Leenders, J.L. Boormans, and C.J. Vissers et al. Antibody EPR3864 is specific for ERG genomic fusions in prostate cancer: implications for pathological practice Mod Pathol 24 2011 1128 1138
23. O. Yaskiv, X. Zhang, and K. Simmerman et al. The utility of ERG/P63 double immunohistochemical staining in the diagnosis of limited cancer in prostate needle biopsies Am J Surg Pathol 35 2011 1062 1068
24. S. Zhang, B. Pavlovitz, J. Tull, Y. Wang, F.M. Deng, and C. Fuller Detection of TMPRSS2 gene deletions and translocations in carcinoma, intraepithelial neoplasia, and normal epithelium of the prostate by direct fluorescence in situ hybridization Diagn Mol Pathol 19 2010 151 156
25. T.A. Bismar, M. Yoshimoto, Q. Duan, S. Liu, K. Sircar, and J.A. Squire Interactions and relationships of PTEN, ERG, SPINK1 and AR in castration-resistant prostate cancer Histopathology 60 2012 645 652
26. F. Demichelis, K. Fall, and S. Perner et al. TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort Oncogene 26 2007 4596 4599
27. S.M. Falzarano, M. Navas, K. Simmerman, E.A. Klein, M.A. Rubin, M. Zhou, and C. Magi-Galluzzi ERG rearrangement is present in a subset of transition zone prostatic tumors Mod Pathol 23 2010 1499 1506
28. S.W. Fine, A. Gopalan, and M.A. Leversha et al. TMPRSS2-ERG gene fusion is associated with low Gleason scores and not with high-grade morphological features Mod Pathol 23 2010 1325 1333
29. A. Gopalan, M.A. Leversha, and M.E. Dudas et al. TMPRSS2-ERG rearrangement in dominant anterior prostatic tumours: incidence and correlation with ERG immunohistochemistry Histopathology 63 2013 279 286
30. S. Liu, M. Yoshimoto, and K. Trpkov et al. Detection of ERG gene rearrangements and PTEN deletions in unsuspected prostate cancer of the transition zone Cancer Biol Ther 11 2011 562 566
31. X. Gao, L.Y. Li, and F.J. Zhou et al. ERG rearrangement for predicting subsequent cancer diagnosis in high-grade prostatic intraepithelial neoplasia and lymph node metastasis Clin Cancer Res 18 2012 4163 4172
32. J.M. Mosquera, S. Perner, and E.M. Genega et al. Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications Clin Cancer Res 14 2008 3380 3385
33. R.B. Shah, Y. Tadros, B. Brummell, and M. Zhou The diagnostic use of ERG in resolving an "atypical glands suspicious for cancer" diagnosis in prostate biopsies beyond that provided by basal cell and alpha-methylacyl-CoA- racemase markers Hum Pathol 44 2013 786 794
34. J. Clark, S. Merson, and S. Jhavar et al. Diversity of TMPRSS2-ERG fusion transcripts in the human prostate Oncogene 26 2007 2667 2673
35. J.P. Clark, and C.S. Cooper ETS gene fusions in prostate cancer Nat Rev Urol 6 2009 429 439
36. M. Braun, D. Goltz, and Z. Shaikhibrahim et al. ERG protein expression and genomic rearrangement status in primary and metastatic prostate cancer - a comparative study of two monoclonal antibodies Prostate Cancer Prostatic Dis 15 2012 165 169
37. K. Park, S.A. Tomlins, and K.M. Mudaliar et al. Antibody-based detection of ERG rearrangement-positive prostate cancer Neoplasia 12 2010 590 598
38. R. Mehra, S.A. Tomlins, and R. Shen et al. Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer Mod Pathol 20 2007 538 544
39. G. Attard, J. Clark, and L. Ambroisine et al. Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer Oncogene 27 2008 253 263
40. A.M. Szasz, A. Majoros, and P. Rosen et al. Prognostic potential of ERG (ETS-related gene) expression in prostatic adenocarcinoma Int Urol Nephrol 45 2013 727 733
41. M.D. Hofer, R. Kuefer, and C. Maier et al. Genome-wide linkage analysis of TMPRSS2-ERG fusion in familial prostate cancer Cancer Res 69 2009 640 646
42. P. Paulo, J.D. Barros-Silva, and F.R. Ribeiro et al. FLI1 is a novel ETS transcription factor involved in gene fusions in prostate cancer Genes Chromosomes Cancer 51 2012 240 249
43. A.B. Rajput, M.A. Miller, and A. De Luca et al. Frequency of the TMPRSS2:ERG gene fusion is increased in moderate to poorly differentiated prostate cancers J Clin Pathol 60 2007 1238 1243
44. B. Furusato, S.H. Tan, and D. Young et al. ERG oncoprotein expression in prostate cancer: clonal progression of ERG-positive tumor cells and potential for ERG-based stratification Prostate Cancer Prostatic Dis 13 2010 228 237
45. A. Pettersson, R.E. Graff, and S.R. Bauer et al. The TMPRSS2:ERG rearrangement, ERG expression, and prostate cancer outcomes: a cohort study and meta-analysis Cancer Epidemiol Biomarkers Prev 21 2012 1497 1509
46. S. Perner, F. Demichelis, and R. Beroukhim et al. TMPRSS2:ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer Cancer Res 66 2006 8337 8341
47. S. Minner, M. Enodien, and H. Sirma et al. ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy Clin Cancer Res 17 2011 5878 5888
48. E.S. Spencer, R.B. Johnston, and R.R. Gordon et al. Prognostic value of ERG oncoprotein in prostate cancer recurrence and cause-specific mortality Prostate 73 2013 905 912
49. M. Yoshimoto, A.M. Joshua, and I.W. Cunha et al. Absence of TMPRSS2:ERG fusions and PTEN losses in prostate cancer is associated with a favorable outcome Mod Pathol 21 2008 1451 1460
50. K. Lee, J.Y. Chae, C. Kwak, J.H. Ku, and K.C. Moon TMPRSS2-ERG gene fusion and clinicopathologic characteristics of Korean prostate cancer patients Urology 76 2010 1268 1313
51. C. Magi-Galluzzi, T. Tsusuki, and P. Elson et al. TMPRSS2-ERG gene fusion prevalence and class are significantly different in prostate cancer of Caucasian African-American and Japanese patients Prostate 71 2011 489 497
52. X. Mao, Y. Yu, and L.K. Boyd et al. Distinct genomic alterations in prostate cancers in Chinese and Western populations suggest alternative pathways of prostate carcinogenesis Cancer Res 70 2010 5207 5212
53. J.L. Boormans, K.G. Hermans, and A.C. Made et al. Expression of the androgen-regulated fusion gene TMPRSS2-ERG does not predict response to endocrine treatment in hormone-naive, node-positive prostate cancer Eur Urol 57 2010 830 835
54. J.D. Barros-Silva, F.R. Ribeiro, and A. Rodrigues et al. Relative 8q gain predicts disease-specific survival irrespective of the TMPRSS2-ERG fusion status in diagnostic biopsies of prostate cancer Genes Chromosomes Cancer 50 2011 662 671
55. G. Schaefer, J.M. Mosquera, and R. Ramoner et al. Distinct ERG rearrangement prevalence in prostate cancer: higher frequency in young age and in low PSA prostate cancer Prostate Cancer Prostatic Dis 16 2013 132 138
56. C. Rouzier, J. Haudebourg, and X. Carpentier et al. Detection of the TMPRSS2-ETS fusion gene in prostate carcinomas: retrospective analysis of 55 formalin-fixed and paraffin-embedded samples with clinical data Cancer Genet Cytogenet 183 2008 21 27
57. Q.P. Sun, L.Y. Li, and Z. Chen et al. Detection of TMPRSS2-ETS fusions by a multiprobe fluorescence in situ hybridization assay for the early diagnosis of prostate cancer: a pilot study J Mol Diagn 12 2010 718 724
58. K.A. Leinonen, T.T. Tolonen, and H. Bracken et al. Association of SPINK1 expression and TMPRSS2:ERG fusion with prognosis in endocrine-treated prostate cancer Clin Cancer Res 16 2010 2845 2851
59. Y. Miyagi, T. Sasaki, and K. Fujinami et al. ETS family-associated gene fusions in Japanese prostate cancer: analysis of 194 radical prostatectomy samples Mod Pathol 23 2010 1492 1498
60. L.M. FitzGerald, I. Agalliu, and K. Johnson et al. Association of TMPRSS2-ERG gene fusion with clinical characteristics and outcomes: results from a population-based study of prostate cancer BMC Cancer 8 2008 230
61. J. Rubio-Briones, A. Fernandez-Serra, and A. Calatrava et al. Clinical implications of TMPRSS2-ERG gene fusion expression in patients with prostate cancer treated with radical prostatectomy J Urol 183 2010 2054 2061
62. K. Kron, L. Liu, and D. Trudel et al. Correlation of ERG expression and DNA methylation biomarkers with adverse clinicopathologic features of prostate cancer Clin Cancer Res 18 2012 2896 2904
63. M. Winnes, E. Lissbrant, J.E. Damber, and G. Stenman Molecular genetic analyses of the TMPRSS2-ERG and TMPRSS2-ETV1 gene fusions in 50 cases of prostate cancer Oncol Rep 17 2007 1033 1036
64. J. Lapointe, Y.H. Kim, and M.A. Miller et al. A variant TMPRSS2 isoform and ERG fusion product in prostate cancer with implications for molecular diagnosis Mod Pathol 20 2007 467 473
65. J. Wang, Y. Cai, C. Ren, and M. Ittmann Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer Cancer Res 66 2006 8347 8351
66. J.J. Tu, S. Rohan, J. Kao, N. Kitabayashi, S. Mathew, and Y.T. Chen Gene fusions between TMPRSS2 and ETS family genes in prostate cancer: frequency and transcript variant analysis by RT-PCR and FISH on paraffin-embedded tissues Mod Pathol 20 2007 921 928
67. L. Bonaccorsi, G. Nesi, and F. Nuti et al. Persistence of expression of the TMPRSS2:ERG fusion gene after pre-surgery androgen ablation may be associated with early prostate specific antigen relapse of prostate cancer: preliminary results J Endocrinol Invest 32 2009 590 596
68. M.A. Svensson, C.J. Lafargue, and T.Y. MacDonald et al. Testing mutual exclusivity of ETS rearranged prostate cancer Lab Invest 91 2011 404 412
69. M. Verdu, I. Trias, and R. Roman et al. ERG expression and prostatic adenocarcinoma Virchows Arch 462 2013 639 644
70. R. Sabaliauskaite, S. Jarmalaite, and D. Petroska et al. Combined analysis of TMPRSS2-ERG and TERT for improved prognosis of biochemical recurrence in prostate cancer Genes Chromosomes Cancer 51 2012 781 791
71. R.B. Nagle, A.M. Algotar, and C.C. Cortez et al. ERG overexpression and PTEN status predict capsular penetration in prostate carcinoma Prostate 73 2013 1233 1240
72. R. Albadine, M. Latour, and A. Toubaji et al. TMPRSS2-ERG gene fusion status in minute (minimal) prostatic adenocarcinoma Mod Pathol 22 2009 1415 1422
73. K.G. Hermans, J.L. Boormans, and D. Gasi et al. Overexpression of prostate-specific TMPRSS2(exon 0)-ERG fusion transcripts corresponds with favorable prognosis of prostate cancer Clin Cancer Res 15 2009 6398 6403
74. A. Toubaji, R. Albadine, and A.K. Meeker et al. Increased gene copy number of ERG on chromosome 21 but not TMPRSS2-ERG fusion predicts outcome in prostatic adenocarcinomas Mod Pathol 24 2011 1511 1520
75. S. Perner, N.J. Rupp, and M. Braun et al. Loss of SLC45A3 protein (prostein) expression in prostate cancer is associated with SLC45A3-ERG gene rearrangement and an unfavorable clinical course Int J Cancer 132 2013 807 812
76. P. Rosen, D. Pfister, and D. Young et al. Differences in frequency of ERG oncoprotein expression between index tumors of Caucasian and African American patients with prostate cancer Urology 80 2012 749 753
77. S.B. Edge, D.R. Byrd, C.C. Compton, A.G. Fritz, F.L. Greene, and A. Trotti AJCC cancer staging manual 2009 Springer
78. D. Hessels, and J.A. Schalken Recurrent gene fusions in prostate cancer: their clinical implications and uses Curr Urol Rep 14 2013 214 222
79. S. Rahim, and A. Uren Emergence of ETS transcription factors as diagnostic tools and therapeutic targets in prostate cancer Am J Transl Res 5 2013 254 268
80. P. Rosen, I.A. Sesterhenn, S.A. Brassell, D.G. McLeod, S. Srivastava, and A. Dobi Clinical potential of the ERG oncoprotein in prostate cancer Nat Rev Urol 9 2012 131 137
81. J.C. Brenner, B. Ateeq, and Y. Li et al. Mechanistic rationale for inhibition of poly(ADP-ribose) polymerase in ETS gene fusion-positive prostate cancer Cancer Cell 19 2011 664 678
82. K. Iljin, M. Wolf, and H. Edgren et al. TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming Cancer Res 66 2006 10242 10246
83. Z. Shaikhibrahim, A. Lindstrot, and J. Ellinger et al. The peripheral zone of the prostate is more prone to tumor development than the transitional zone: is the ETS family the key? Mol Med Rep 5 2012 313 316
84. R. Mehra, B. Han, and S.A. Tomlins et al. Heterogeneity of TMPRSS2 gene rearrangements in multifocal prostate adenocarcinoma: molecular evidence for an independent group of diseases Cancer Res 67 2007 7991 7995
85. S. Minner, M. Gartner, and F. Freudenthaler et al. Marked heterogeneity of ERG expression in large primary prostate cancers Mod Pathol 26 2013 106 116
86. A. Ingels, A. de la Taille, and G. Ploussard Radical prostatectomy as primary treatment of high-risk prostate cancer Curr Urol Rep 13 2012 179 186