Abstract
Recurrent gene fusions between the androgen-regulated gene TMPRSS2 and the ETS transcription factor family members ERG, ETV1, and ETV4 have been identified as a critical event in prostate cancer development. In this study, we characterized the prevalence and diversity of these rearrangements in hormone-refractory metastatic prostate cancer. We used a fluorescence in situ hybridization (FISH) split probe strategy to comprehensively evaluate TMPRSS2-ETS aberrations across 97 nonosseous metastatic sites of prostate cancer from 30 rapid autopsies of men who died of androgen-independent disease. Tissue microarrays were constructed representing multiple metastatic sites from each patient, and split signal FISH probes for TMPRSS2, ERG, ETV1, and ETV4 were used to assess for TMPRSS2-ETS rearrangements. In patients exhibiting these aberrations, multiple sites from an individual case harbored the same gene fusion molecular subtype suggesting clonal expansion of disease. The most common prostate cancer gene fusion, TMPRSS2-ERG, can be generated by the mechanism of interstitial deletion (Edel) about 39% to 60% of the time in clinically localized disease. Interestingly, we observed that all of the androgen-independent metastatic prostate cancer sites harboring TMPRSS2-ERG were associated with Edel. These findings suggest that TMPRSS2-ERG with Edel is an aggressive and, in this study, uniformly lethal molecular subtype of prostate cancer associated with androgen-independent disease.
MeSH Terms
Androgens/metabolism
Chromosome Aberrations
Cohort Studies
Gene Deletion
Humans
In Situ Hybridization, Fluorescence
Male
Models, Genetic
Mutation
Neoplasm Metastasis
Oncogene Proteins, Fusion/genetics,physiology
Prostatic Neoplasms/genetics
Proto-Oncogene Proteins c-ets/genetics
Serine Endopeptidases/genetics,physiology
Trans-Activators/genetics
Transcriptional Regulator ERG
Chemicals
Androgens
ERG protein, human
Oncogene Proteins, Fusion
Proto-Oncogene Proteins c-ets
Trans-Activators
Transcriptional Regulator ERG
Serine Endopeptidases
TMPRSS2 protein, human
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Mehra Rohit
Michigan Center for Translational Pathology, Department of Pathology, University of Michigan Medical School, Ann Arbor, Michigan, USA.
Tomlins Scott A
Yu Jianjun
Cao Xuhong
Wang Lei
Menon Anjana
Rubin Mark A
Pienta Kenneth J
Shah Rajal B
Chinnaiyan Arul M
References (22)
22 references, click to expand
-
TMPRSS2:ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer.
Cancer Res. 2006 Sep 1;66(17):8337-41
PMID: 16951139
-
Diversity of TMPRSS2-ERG fusion transcripts in the human prostate.
Oncogene. 2007 Apr 19;26(18):2667-73
PMID: 17043636
-
Heterogeneity of TMPRSS2 gene rearrangements in multifocal prostate adenocarcinoma: molecular evidence for an independent group of diseases.
Cancer Res. 2007 Sep 1;67(17):7991-5
PMID: 17804708
-
Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer.
Cancer Res. 2006 Sep 1;66(17):8347-51
PMID: 16951141
-
Complex patterns of ETS gene alteration arise during cancer development in the human prostate.
Oncogene. 2008 Mar 27;27(14):1993-2003
PMID: 17922029
-
TMPRSS2:ETV4 gene fusions define a third molecular subtype of prostate cancer.
Cancer Res. 2006 Apr 1;66(7):3396-400
PMID: 16585160
-
Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program.
Cancer Res. 2004 Dec 15;64(24):9209-16
PMID: 15604294
-
TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming.
Cancer Res. 2006 Nov 1;66(21):10242-6
PMID: 17079440
-
Genetic alterations in untreated metastases and androgen-independent prostate cancer detected by comparative genomic hybridization and allelotyping.
Cancer Res. 1996 Jul 1;56(13):3091-102
PMID: 8674067
-
A variant TMPRSS2 isoform and ERG fusion product in prostate cancer with implications for molecular diagnosis.
Mod Pathol. 2007 Apr;20(4):467-73
PMID: 17334351
-
Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer.
Science. 2005 Oct 28;310(5748):644-8
PMID: 16254181
-
Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer.
Genes Chromosomes Cancer. 2006 Jul;45(7):717-9
PMID: 16575875
-
Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer.
Mod Pathol. 2007 May;20(5):538-44
PMID: 17334343
-
Heterogeneity of Gleason grade in multifocal adenocarcinoma of the prostate.
Cancer. 2004 Jun 1;100(11):2362-6
PMID: 15160339
-
The evolving biology and treatment of prostate cancer.
J Clin Invest. 2007 Sep;117(9):2351-61
PMID: 17786228
-
Expression of TMPRSS2:ERG gene fusion in prostate cancer cells is an important prognostic factor for cancer progression.
Cancer Biol Ther. 2007 Jan;6(1):40-5
PMID: 17172822
-
TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort.
Oncogene. 2007 Jul 5;26(31):4596-9
PMID: 17237811
-
TMPRSS2:ERG fusion by translocation or interstitial deletion is highly relevant in androgen-dependent prostate cancer, but is bypassed in late-stage androgen receptor-negative prostate cancer.
Cancer Res. 2006 Nov 15;66(22):10658-63
PMID: 17108102
-
Rapid ("warm") autopsy study for procurement of metastatic prostate cancer.
Clin Cancer Res. 2000 Mar;6(3):1038-45
PMID: 10741732
-
Distinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer.
Nature. 2007 Aug 2;448(7153):595-9
PMID: 17671502
-
Frequency of the TMPRSS2:ERG gene fusion is increased in moderate to poorly differentiated prostate cancers.
J Clin Pathol. 2007 Nov;60(11):1238-43
PMID: 17259299
-
Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer.
Oncogene. 2008 Jan 10;27(3):253-63
PMID: 17637754