TMPRSS2/ERG promotes epithelial to mesenchymal transition through the ZEB1/ZEB2 axis in a prostate cancer model

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Leshem, Orit ^a,b   Madar, Shalom ^c   Kogan Sakin, Ira ^c   Kamer, Iris ^c   Goldstein, Ido ^c   Brosh, Ran ^c   Cohen, Yehudit ^a   Jacob Hirsch, Jasmine ^a   Ehrlich, Marcelo ^d   Ben Sasson, Shmuel ^b   Goldfinger, Naomi ^c   Loewenthal, Ron ^a   Gazit, Ephraim ^a   Rotter, Varda ^c   Berger, Raanan ^a  

^a SHEBA MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

UVOMORULIN; VIMENTIN; HOMEODOMAIN PROTEIN; REPRESSOR PROTEIN; SERINE PROTEINASE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; ZEB1 PROTEIN, HUMAN; ZEB2 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CARCINOGENESIS; CELL IMMORTALIZATION; CELL INVASION; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE FUSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ILR2 GENE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROMOTER REGION; PROSTATE CANCER; PROSTATE EPITHELIUM; SHORT TANDEM REPEAT; SPINT1 GENE; TMPRSS2 ERG GENE FUSION; UPREGULATION; ZEB1 GENE; ZEB2 GENE; ANIMAL; CELL LINE; DISEASE MODEL; GENE VECTOR; GENETICS; MALE; METABOLISM; PATHOLOGY; PHENOTYPE; PROSTATE TUMOR; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; EPITHELIAL-MESENCHYMAL TRANSITION; GENE FUSION; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; PHENOTYPE; PROSTATIC NEOPLASMS; REPRESSOR PROTEINS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 79959829839     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021650     Document Type: Article

References (47)

1. Tomlins SA, Bjartell A, Chinnaiyan AM, Jenster G, Nam RK, et al. (2009) ETS gene fusions in prostate cancer: from discovery to daily clinical practice. Eur Urol 56: 275-286.
2. Yoshimoto M, Joshua AM, Chilton-Macneill S, Bayani J, Selvarajah S, et al. (2006) Three-color FISH analysis of TMPRSS2/ERG fusions in prostate cancer indicates that genomic microdeletion of chromosome 21 is associated with rearrangement. Neoplasia 8: 465-469.
3. Hermans KG, van Marion R, van Dekken H, Jenster G, van Weerden WM, et al. (2006) 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 66: 10658-10663.
4. Teixeira MR, (2008) Chromosome mechanisms giving rise to the TMPRSS2-ERG fusion oncogene in prostate cancer and HGPIN lesions. Am J Surg Pathol 32: 642-644 author reply 644.
5. Perner S, Mosquera JM, Demichelis F, Hofer MD, Paris PL, et al. (2007) TMPRSS2-ERG fusion prostate cancer: an early molecular event associated with invasion. Am J Surg Pathol 31: 882-888.
6. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, et al. (2005) Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310: 644-648.
7. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM, (2008) Recurrent gene fusions in prostate cancer. Nat Rev Cancer 8: 497-511.
8. Demichelis F, Fall K, Perner S, Andren O, Schmidt F, et al. (2007) TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene 26: 4596-4599.
9. Attard G, Clark J, Ambroisine L, Fisher G, Kovacs G, et al. (2008) Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene 27: 253-263.
10. Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, et al. (2008) Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 10: 177-188.
11. Carver BS, Tran J, Chen Z, Carracedo-Perez A, Alimonti A, et al. (2009) ETS rearrangements and prostate cancer initiation. Nature: 457: E1; discussion E2-3.
12. Saramaki OR, Harjula AE, Martikainen PM, Vessella RL, Tammela TL, et al. (2008) TMPRSS2:ERG fusion identifies a subgroup of prostate cancers with a favorable prognosis. Clin Cancer Res 14: 3395-3400.
13. Wang J, Cai Y, Yu W, Ren C, Spencer DM, et al. (2008) Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res 68: 8516-8524.
14. Sun C, Dobi A, Mohamed A, Li H, Thangapazham RL, et al. (2008) TMPRSS2-ERG fusion, a common genomic alteration in prostate cancer activates C-MYC and abrogates prostate epithelial differentiation. Oncogene 27: 5348-5353.
15. Klezovitch O, Risk M, Coleman I, Lucas JM, Null M, et al. (2008) A causal role for ERG in neoplastic transformation of prostate epithelium. Proc Natl Acad Sci U S A 105: 2105-2110.
16. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, et al. (2009) Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 41: 524-526.
17. Iljin K, Wolf M, Edgren H, Gupta S, Kilpinen S, et al. (2006) TMPRSS2 fusions with oncogenic ETS factors in prostate cancer involve unbalanced genomic rearrangements and are associated with HDAC1 and epigenetic reprogramming. Cancer Res 66: 10242-10246.
18. Bjorkman M, Iljin K, Halonen P, Sara H, Kaivanto E, et al. (2008) Defining the molecular action of HDAC inhibitors and synergism with androgen deprivation in ERG-positive prostate cancer. Int J Cancer 123: 2774-2781.
19. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, et al. (2009) Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 41: 619-624.
20. Zong Y, Xin L, Goldstein AS, Lawson DA, Teitell MA, et al. (2009) ETS family transcription factors collaborate with alternative signaling pathways to induce carcinoma from adult murine prostate cells. Proc Natl Acad Sci U S A 106: 12465-12470.
21. Gupta S, Iljin K, Sara H, Mpindi JP, Mirtti T, et al. (2010) FZD4 as a Mediator of ERG Oncogene-Induced WNT Signaling and Epithelial-to-Mesenchymal Transition in Human Prostate Cancer Cells. Cancer Res.
22. Berger R, Febbo PG, Majumder PK, Zhao JJ, Mukherjee S, et al. (2004) Androgen-induced differentiation and tumorigenicity of human prostate epithelial cells. Cancer Res 64: 8867-8875.
23. Cai C, Wang H, Xu Y, Chen S, Balk SP, (2009) Reactivation of androgen receptor-regulated TMPRSS2:ERG gene expression in castration-resistant prostate cancer. Cancer Res 69: 6027-6032.
24. Mertz KD, Setlur SR, Dhanasekaran SM, Demichelis F, Perner S, et al. (2007) Molecular characterization of TMPRSS2-ERG gene fusion in the NCI-H660 prostate cancer cell line: a new perspective for an old model. Neoplasia 9: 200-206.
25. Ikenouchi J, Matsuda M, Furuse M, Tsukita S, (2003) Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 116: 1959-1967.
26. Ke XS, Qu Y, Goldfinger N, Rostad K, Hovland R, et al. (2008) Epithelial to mesenchymal transition of a primary prostate cell line with switches of cell adhesion modules but without malignant transformation. PLoS One 3: e3368.
27. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
28. Cerveira N, Ribeiro FR, Peixoto A, Costa V, Henrique R, et al. (2006) TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia 8: 826-832.
29. Darnel AD, Lafargue CJ, Vollmer RT, Corcos J, Bismar TA, (2009) TMPRSS2-ERG fusion is frequently observed in Gleason pattern 3 prostate cancer in a Canadian cohort. Cancer Biol Ther 8: 125-130.
30. Mosquera JM, Perner S, Genega EM, Sanda M, Hofer MD, et al. (2008) Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications. Clin Cancer Res 14: 3380-3385.
31. Edwards A, Civitello A, Hammond HA, Caskey CT, (1991) DNA typing and genetic mapping with trimeric and tetrameric tandem repeats. Am J Hum Genet 49: 746-756.
32. Edwards A, Hammond HA, Jin L, Caskey CT, Chakraborty R, (1992) Genetic variation at five trimeric and tetrameric tandem repeat loci in four human population groups. Genomics 12: 241-253.
33. Evett IW, Gill PD, Scrange JK, Weir BS, (1996) Establishing the robustness of short-tandem-repeat statistics for forensic applications. Am J Hum Genet 58: 398-407.
34. Hammond HA, Jin L, Zhong Y, Caskey CT, Chakraborty R, (1994) Evaluation of 13 short tandem repeat loci for use in personal identification applications. Am J Hum Genet 55: 175-189.
35. Chang SY, Su PF, Lee TC, (2009) Ectopic expression of interleukin-1 receptor type II enhances cell migration through activation of the pre-interleukin 1alpha pathway. Cytokine 45: 32-38.
36. Cheng H, Fukushima T, Takahashi N, Tanaka H, Kataoka H, (2009) Hepatocyte growth factor activator inhibitor type 1 regulates epithelial to mesenchymal transition through membrane-bound serine proteinases. Cancer Res 69: 1828-1835.
37. Drake JM, Strohbehn G, Bair TB, Moreland JG, Henry MD, (2009) ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells. Mol Biol Cell 20: 2207-2217.
38. Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, et al. (2008) Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 68: 2479-2488.
39. Kong D, Li Y, Wang Z, Banerjee S, Ahmad A, et al. (2009) miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 27: 1712-1721.
40. Pena C, Garcia JM, Garcia V, Silva J, Dominguez G, et al. (2006) The expression levels of the transcriptional regulators p300 and CtBP modulate the correlations between SNAIL, ZEB1, E-cadherin and vitamin D receptor in human colon carcinomas. Int J Cancer 119: 2098-2104.
41. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, et al. (2008) Epithelial to mesenchymal transition (EMT) in human prostate cancer: lessons learned from ARCaP model. Clin Exp Metastasis 25: 601-610.
42. Zhu ML, Kyprianou N, (2009) Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. Faseb J.
43. Ma Y, Visser L, Roelofsen H, de Vries M, Diepstra A, et al. (2008) Proteomics analysis of Hodgkin lymphoma: identification of new players involved in the cross-talk between HRS cells and infiltrating lymphocytes. Blood 111: 2339-2346.
44. Saleem M, Adhami VM, Zhong W, Longley BJ, Lin CY, et al. (2006) A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol Biomarkers Prev 15: 217-227.
45. Sanders AJ, Parr C, Mason MD, Jiang WG, (2007) Suppression of hepatocyte growth factor activator inhibitor-1 leads to a more aggressive phenotype of prostate cancer cells in vitro. Int J Mol Med 20: 613-619.
46. Madar S, Brosh R, Buganim Y, Ezra O, Goldstein I, et al. (2009) Modulated expression of WFDC1 during carcinogenesis and cellular senescence. Carcinogenesis 30: 20-27.
47. Genomatix website, available at: www.genomatix.de Accessed 2010 March 1st.