The discovery of common recurrent transmembrane protease serine 2 (TMPRSS2)-erythroblastosis virus E26 transforming sequence (ETS) gene fusions in prostate cancer: Significance and clinical implications

Advances in Anatomic Pathology

Volumn 16, Issue 3, 2009, Pages 145-153

  Shah, Rajal B ^a   Chinnaiyan, Arul M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Biomarkers; Gene fusions; Prostate cancer

Indexed keywords

ANDROGEN; PROSTATE SPECIFIC ANTIGEN; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR ETS; TRANSMEMBRANE PROTEASE SERINE 2; TUMOR PROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; ONCOPROTEIN; TMPRSS2 ETS FUSION PROTEIN, HUMAN; TMPRSS2-ETS FUSION PROTEIN, HUMAN;

ANTIGEN DETECTION; BIOINFORMATICS; CANCER GROWTH; CANCER LOCALIZATION; CANCER SURGERY; CANCER SURVIVAL; CHROMOSOME REARRANGEMENT; EARLY DIAGNOSIS; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE FUSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HEMATOLOGIC MALIGNANCY; HISTOPATHOLOGY; MALE; MOLECULAR DYNAMICS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER; PROTEIN TARGETING; REGULATOR GENE; REVIEW; SARCOMA; TISSUE STRUCTURE; TREATMENT OUTCOME; BIOLOGY; CANCER DIAGNOSIS; CHROMOSOME 21; CHROMOSOME ABERRATION; GENE EXPRESSION; GENETICS; HUMAN; METASTASIS; PATHOLOGY; PROSTATE TUMOR;

BIOLOGICAL MARKERS; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 21; COMPUTATIONAL BIOLOGY; EARLY DETECTION OF CANCER; GENE EXPRESSION; GENE FUSION; HUMANS; MALE; NEOPLASM METASTASIS; ONCOGENE PROTEINS, FUSION; PROGNOSIS; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS;

EID: 66349115692     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/PAP.0b013e3181a12da7     Document Type: Review

References (65)

1. Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer. 2007;7:233-245. (Pubitemid 46480968)
2. Rabbitts TH. Chromosomal translocations in human cancer. Nature. 1994;372:143-149.
3. Rowley JD. Chromosome translocations: dangerous liaisons revisited. Nat Rev Cancer. 2001;1:245-250.
4. Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer. 2005;5:172-183. (Pubitemid 40314949)
5. Mitelman F, Johansson B, Mertens F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nat Genet. 2004;36:331-334. (Pubitemid 38437252)
6. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. Recurrent gene fusions in prostate cancer. Nat Rev Cancer. 2008;8:497-511.
7. Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644-648. (Pubitemid 41528150)
8. Morris DS, Tomlins SA, Montie JE, et al. The discovery and application of gene fusions in prostate cancer. BJU Int. 2008;102:276-282. (Pubitemid 352019201)
9. Rubin MA, Chinnaiyan AM. Bioinformatics approach leads to the discovery of the TMPRSS2: ETS gene fusion in prostate cancer. Lab Invest. 2006;86:1099-1102.
10. Hsu T, Trojanowska M, Watson DK. Ets proteins in biological control and cancer. J Cell Biochem. 2004;91:896-903.
11. Oikawa T, Yamada T. Molecular biology of the Ets family of transcription factors. Gene. 2003;303:11-34. (Pubitemid 36151767)
12. Cerveira N, Ribeiro FR, Peixoto A, et al. TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia. 2006;8:826-832. (Pubitemid 44564838)
13. Demichelis F, Fall K, Perner S, et al. TMPRSS2: ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene. 2007;26:4596-4599. (Pubitemid 47037039)
14. Hermans KG, van Marion R, van Dekken H, et al. 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;66:10658-10663.
15. Iljin K, Wolf M, Edgren H, 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. 2006;66:10242-10246. (Pubitemid 44799738)
16. Lapointe J, Kim YH, Miller MA, et al. A variant TMPRSS2 isoform and ERG fusion product in prostate cancer with implications for molecular diagnosis. Mod Pathol. 2007;20:467-473. (Pubitemid 46482370)
17. Mehra R, Tomlins SA, Shen R, et al. Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer. Mod Pathol. 2007;20:538-544. (Pubitemid 46631996)
18. Mosquera JM, Perner S, Demichelis F, et al. Morphological features of TMPRSS2-ERG gene fusion prostate cancer. J Pathol. 2007;212:91-101. (Pubitemid 46746294)
19. Nami RK, Sugar L, Wang Z, et al. Expression of TMPRSS2: ERG gene fusion in prostate cancer cells is an important prognostic factor for cancer progression. Cancer Biol Ther. 2007;6:40-45. (Pubitemid 46294173)
20. Perner S, Demichelis F, Beroukhim R, et al. TMPRSS2: ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer. Cancer Res. 2006;66:8337-8341. (Pubitemid 44449140)
21. Rajput AB, Miller MA, De Luca A, et al. Frequency of the TMPRSS2: ERG gene fusion is increased in moderate to poorly differentiated prostate cancers. J Clin Pathol. 2007;60:1238-1243. (Pubitemid 350084545)
22. Soller MJ, Isaksson M, Elfving P, et al. Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer. Genes Chromosomes Cancer. 2006;45:717-719. (Pubitemid 43727158)
23. Tu JJ, Rohan S, Kao J, et al. 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. 2007;20:921-928. (Pubitemid 47267823)
24. Wang J, Cai Y, Ren C, et al. Expression of variant TMPRSS2/ ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res. 2006;66:8347-8351. (Pubitemid 44449142)
25. Winnes M, Lissbrant E, Damber JE, et al. Molecular genetic analyses of the TMPRSS2-ERG and TMPRSS2-ETV1 gene fusions in 50 cases of prostate cancer. Oncol Rep. 2007;17:1033-1036.
26. Yoshimoto M, Joshua AM, Chilton-Macneill S, et al. Threecolor FISH analysis of TMPRSS2/ERG fusions in prostate cancer indicates that genomic microdeletion of chromosome 21 is associated with rearrangement. Neoplasia. 2006;8:465-469. (Pubitemid 44035330)
27. Han B, Mehra R, Dhanasekaran SM, et al. A fluorescence in situ hybridization screen for E26 transformation-specific aberrations: identification of DDX5-ETV4 fusion protein in prostate cancer. Cancer Res. 2008;68:7629-7637.
28. Setlur SR, Mertz KD, Hoshida Y, et al. Estrogen-dependent signaling in a molecularly distinct subclass of aggressive prostate cancer. J Natl Cancer Inst. 2008;100:815-825. (Pubitemid 351809667)
29. Mehra R, Han B, Tomlins SA, et al. Heterogeneity of TMPRSS2 gene rearrangements in multifocal prostate adenocarcinoma: molecular evidence for an independent group of diseases. Cancer Res. 2007;67:7991-7995. (Pubitemid 47395131)
30. Mehra R, Tomlins SA, Yu J, et al. Characterization of TMPRSS2-ETS gene aberrations in androgen-independent metastatic prostate cancer. Cancer Res. 2008;68:3584-3590.
31. Clark J, Attard G, Jhavar S, et al. Complex patterns of ETS gene alteration arise during cancer development in the human prostate. Oncogene. 2008;27:1993-2003.
32. Helgeson BE, Tomlins SA, Shah N, et al. Characterization of TMPRSS2: ETV5 and SLC45A3:ETV5 gene fusions in prostate cancer. Cancer Res. 2008;68:73-80.
33. Tomlins SA, Laxman B, Dhanasekaran SM, et al. Distinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer. Nature. 2007;448:595-599. (Pubitemid 47206938)
34. Tomlins SA, Mehra R, Rhodes DR, et al. TMPRSS2: ETV4 gene fusions define a third molecular subtype of prostate cancer. Cancer Res. 2006;66:3396-3400.
35. Hermans KG, Bressers AA, van der Korput HA, et al. Two unique novel prostate-specific and androgen-regulated fusion partners of ETV4 in prostate cancer. Cancer Res. 2008;68:3094-3098.
36. Tomlins SA, Rhodes DR, Yu J, et al. The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell. 2008;13:519-528. (Pubitemid 351763901)
37. Arora R, Koch MO, Eble JN, et al. Heterogeneity of Gleason grade in multifocal adenocarcinoma of the prostate. Cancer. 2004;100:2362-2366. (Pubitemid 38657883)
38. Tomlins SA, Mehra R, Rhodes DR, et al. Integrative molecular concept modeling of prostate cancer progression. Nat Genet. 2007;39:41-51. (Pubitemid 46026500)
39. Barry M, Perner S, Demichelis F, et al. TMPRSS2-ERG fusion heterogeneity in multifocal prostate cancer: clinical and biologic implications. Urology. 2007;70:630-633. (Pubitemid 350030260)
40. Clark J, Merson S, Jhavar S, et al. Diversity of TMPRSS2- ERG fusion transcripts in the human prostate. Oncogene. 2007;26:2667-2673. (Pubitemid 46632014)
41. DeMarzo AM, Nelson WG, Isaacs WB, et al. Pathological and molecular aspects of prostate cancer. Lancet. 2003;361:955-964. (Pubitemid 36332115)
42. Klezovitch O, Risk M, Coleman I, et al. A causal role for ERG in neoplastic transformation of prostate epithelium. Proc Natl Acad Sci U S A. 2008;105:2105-2110.
43. Perner S, Mosquera JM, Demichelis F, et al. TMPRSS2-ERG fusion prostate cancer: an early molecular event associated with invasion. Am J Surg Pathol. 2007;31:882-888. (Pubitemid 47165141)
44. Tomlins SA, Laxman B, Varambally S, et al. Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia. 2008;10:177-188. (Pubitemid 351240884)
45. Mosquera JM, Perner S, Genega EM, et al. Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications. Clin Cancer Res. 2008;14:3380-3385.
46. Shah RB, Mehra R, Chinnaiyan AM, et al. Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program. Cancer Res. 2004;64:9209-9216. (Pubitemid 39665537)
47. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2007. CA Cancer J Clin. 2007;57:43-66.
48. Bailar JC III, Mellinger GT, Gleason DF. Survival rates of patients with prostatic cancer, tumor stage, and differentiation - preliminary report. Cancer Chemother Rep. 1966;50:129-136.
49. Johansson JE, Adami HO, Andersson SO, et al. Natural history of localised prostatic cancer. A population-based study in 223 untreated patients. Lancet. 1989;1:799-803.
50. Attard G, Clark J, Ambroisine L, et al. Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene. 2008;27:253-263.
51. Petrovics G, Liu A, Shaheduzzaman S, et al. Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene. 2005;24:3847-3852. (Pubitemid 40826884)
52. Alexander J, Watanabe T, Wu TT, et al. Histopathological identification of colon cancer with microsatellite instability. Am J Pathol. 2001;158:527-535. (Pubitemid 32158613)
53. Greenson JK, Bonner JD, Ben-Yzhak O, et al. Phenotype of microsatellite unstable colorectal carcinomas: well-differentiated and focally mucinous tumors and the absence of dirty necrosis correlate with microsatellite instability. Am J Surg Pathol. 2003;27:563-570. (Pubitemid 36514468)
54. Lakhani SR. The pathology of familial breast cancer: Morphological aspects. Breast Cancer Res. 1999;1:31-35. (Pubitemid 32223533)
55. Lakhani SR, Jacquemier J, Sloane JP, et al. Multifactorial analysis of differences between sporadic breast cancers and cancers involving BRCA1 and BRCA2 mutations. J Natl Cancer Inst. 1998;90:1138-1145. (Pubitemid 28380718)
56. Argani P, Antonescu CR, Couturier J, et al. PRCC-TFE3 renal carcinomas: morphologic, immunohistochemical, ultrastructural, and molecular analysis of an entity associated with the t(X;1)(p11.2;q21). Am J Surg Pathol. 2002;26:1553-1566. (Pubitemid 35387219)
57. Wu A, Kunju LP, Cheng L, et al. Renal cell carcinoma in children and young adults: analysis of clinicopathological, immunohistochemical and molecular characteristics with an emphasis on the spectrum of Xp11.2 translocation- associated and unusual clear cell subtypes. Histopathology. 2008;53:533-544.
58. Brawer MK, Chetner MP, Beatie J, et al. Screening for prostatic carcinoma with prostate specific antigen. J Urol. 1992;147(3 Pt 2):841-845.
59. Catalona WJ, Smith DS, Ratliff TL, et al. Measurement of prostate-specific antigen in serum as a screening test for prostate cancer. N Engl J Med. 1991;324:1156-1161.
60. Brawley OW, Knopf K, Merrill R. The epidemiology of prostate cancer part I: descriptive epidemiology. Semin Urol Oncol. 1998;16:187-192. (Pubitemid 28553364)
61. Thompson IM, Pauler DK, Goodman PJ, et al. Prevalence of prostate cancer among men with a prostate-specific antigen level r4.0 ng per milliliter. N Engl J Med. 2004;350:2239-2246.
62. Mao X, Shaw G, James SY, et al. Detection of TMPRSS2: ERG fusion gene in circulating prostate cancer cells. Asian J Androl. 2008;10:467-473. (Pubitemid 351596036)
63. Laxman B, Tomlins SA, Mehra R, et al. Noninvasive detection of TMPRSS2: ERG fusion transcripts in the urine of men with prostate cancer. Neoplasia. 2006;8:885-888.
64. Laxman B, Morris DS, Yu J, et al. A first-generation multiplex biomarker analysis of urine for the early detection of prostate cancer. Cancer Res. 2008;68:645-649. (Pubitemid 351206738)
65. Hessels D, Smit FP, Verhaegh GW, et al. Detection of TMPRSS2-ERG fusion transcripts and prostate cancer antigen 3 in urinary sediments may improve diagnosis of prostate cancer. Clin Cancer Res. 2007;13:5103-5108. (Pubitemid 47502077)