Loss of the NKX3.1 tumorsuppressor promotes the TMPRSS2-ERG fusion gene expression in prostate cancer

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Thangapazham, Rajesh ^a   Saenz, Francisco ^a   Katta, Shilpa ^a   Mohamed, Ahmed A ^a   Tan, Shyh Han ^a   Petrovics, Gyorgy ^a   Srivastava, Shiv ^a   Dobi, Albert ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

ERG; NFk cyrillic B; NKX3.1; Oncogene; Prostate; Tumor suppressor

Indexed keywords

NK3 HOMEOBOX 1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARCINOGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ERG GENE; GENE; GENE EXPRESSION; GENE FUSION; GENE SEQUENCE; HUMAN; HUMAN CELL; MALE; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROSTATE CANCER; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TMPRSS2 GENE;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE FUSION; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; MALE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; ONCOGENE PROTEINS, FUSION; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; RNA INTERFERENCE; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84892429204     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-16     Document Type: Article

References (51)

1. Reddy ES, Rao VN, Papas TS. The erg gene: a human gene related to the ets oncogene. Proc Natl Acad Sci USA 1987, 84(17):6131-6135. 10.1073/pnas.84.17.6131, 299022, 3476934.
2. Rahim S, Uren A. Emergence of ETS transcription factors as diagnostic tools and therapeutic targets in prostate cancer. Am J of Transl Res 2013, 5(3):254-268.
3. Barbieri CE, Bangma CH, Bjartell A, Catto JW, Culig Z, Gronberg H, Luo J. Visakorpi T 2013, The Mutational Landscape of Prostate Cancer. European urology: Rubin MA.
4. Hessels D, Schalken JA. Recurrent gene fusions in prostate cancer: their clinical implications and uses. Curr Urol Rep 2013, 14(3):214-222. 10.1007/s11934-013-0321-1, 23625457.
5. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. Recurrent gene fusions in prostate cancer. Nat Rev Cancer 2008, 8(7):497-511. 10.1038/nrc2402, 2711688, 18563191.
6. Rubin MA. ETS rearrangements in prostate cancer. Asian J of Androl 2012, 14(3):393-399.
7. Furusato B, Tan SH, Young D, Dobi A, Sun C, Mohamed AA, Thangapazham R, Chen Y, McMaster G, Sreenath T, et al. ERG oncoprotein expression in prostate cancer: clonal progression of ERG-positive tumor cells and potential for ERG-based stratification. Prostate cancer and prostatic Dis 2010, 13(3):228-237.
8. Park K, Tomlins SA, Mudaliar KM, Chiu YL, Esgueva R, Mehra R, Suleman K, Varambally S, Brenner JC, MacDonald T, et al. Antibody-based detection of ERG rearrangement-positive prostate cancer. Neoplasia 2010, 12(7):590-598. 2907585, 20651988.
9. Lin B, Ferguson C, White JT, Wang S, Vessella R, True LD, Hood L, Nelson PS. Prostate-localized and androgen-regulated expression of the membrane-bound serine protease TMPRSS2. Cancer Res 1999, 59(17):4180-4184.
10. Agoulnik IU, Weigel NL. Coactivator selective regulation of androgen receptor activity. Steroids 2009, 74(8):669-674. 10.1016/j.steroids.2009.02.007, 2687407, 19463689.
11. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310(5748):644-648. 10.1126/science.1117679, 16254181.
12. Pignon JC, Koopmansch B, Nolens G, Delacroix L, Waltregny D, Winkler R. Androgen receptor controls EGFR and ERBB2 gene expression at different levels in prostate cancer cell lines. Cancer Res 2009, 69(7):2941-2949. 10.1158/0008-5472.CAN-08-3760, 19318561.
13. Welsbie DS, Xu J, Chen Y, Borsu L, Scher HI, Rosen N, Sawyers CL. Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer. Cancer Res 2009, 69(3):958-966. 10.1158/0008-5472.CAN-08-2216, 3219545, 19176386.
14. Chen H, Nandi AK, Li X, Bieberich CJ. NKX-3.1 interacts with prostate-derived Ets factor and regulates the activity of the PSA promoter. Cancer Res 2002, 62(2):338-340.
15. Abate-Shen C, Shen MM, Gelmann E. Integrating differentiation and cancer: the Nkx3.1 homeobox gene in prostate organogenesis and carcinogenesis. Differ; Res in Biol diversity 2008, 76(6):717-727.
16. Iwata T, Schultz D, Hicks J, Hubbard GK, Mutton LN, Lotan TL, Bethel C, Lotz MT, Yegnasubramanian S, Nelson WG, et al. MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PloS one 2010, 5(2):e9427. 10.1371/journal.pone.0009427, 2828486, 20195545.
17. Kim MJ, Cardiff RD, Desai N, Banach-Petrosky WA, Parsons R, Shen MM, Abate-Shen C. Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc Natl Acad Sci USA 2002, 99(5):2884-2889. 10.1073/pnas.042688999, 122442, 11854455.
18. Abate-Shen C, Banach-Petrosky WA, Sun X, Economides KD, Desai N, Gregg JP, Borowsky AD, Cardiff RD, Shen MM. Nkx3.1; Pten mutant mice develop invasive prostate adenocarcinoma and lymph node metastases. Cancer Res 2003, 63(14):3886-3890.
19. Song H, Zhang B, Watson MA, Humphrey PA, Lim H, Milbrandt J. Loss of Nkx3.1 leads to the activation of discrete downstream target genes during prostate tumorigenesis. Oncogene 2009, 28(37):3307-3319. 10.1038/onc.2009.181, 2746257, 19597465.
20. Bowen C, Gelmann EP. NKX3.1 activates cellular response to DNA damage. Cancer Res 2010, 70(8):3089-3097. 10.1158/0008-5472.CAN-09-3138, 20395202.
21. Anderson PD, McKissic SA, Logan M, Roh M, Franco OE, Wang J, Doubinskaia I, van der Meer R, Hayward SW, Eischen CM, et al. Nkx3.1 and Myc crossregulate shared target genes in mouse and human prostate tumorigenesis. The J of Clin Invest 2012, 122(5):1907-1919.
22. Sun C, Dobi A, Mohamed A, Li H, Thangapazham RL, Furusato B, Shaheduzzaman S, Tan SH, Vaidyanathan G, Whitman E, et al. TMPRSS2-ERG fusion, a common genomic alteration in prostate cancer activates C-MYC and abrogates prostate epithelial differentiation. Oncogene 2008, 27(40):5348-5353. 10.1038/onc.2008.183, 18542058.
23. Zong Y, Xin L, Goldstein AS, Lawson DA, Teitell MA, Witte ON. ETS family transcription factors collaborate with alternative signaling pathways to induce carcinoma from adult murine prostate cells. Proc Natl Acad Sci USA 2009, 106(30):12465-12470. 10.1073/pnas.0905931106, 2708977, 19592505.
24. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH, Taylor BS, Sander C, Cardiff RD, Couto SS, et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 2009, 41(5):524-526. 10.1038/ng.371, 2898503, 19396167.
25. Kunderfranco P, Mello-Grand M, Cangemi R, Pellini S, Mensah A, Albertini V, Malek A, Chiorino G, Catapano CV, Carbone GM. ETS transcription factors control transcription of EZH2 and epigenetic silencing of the tumor suppressor gene Nkx3.1 in prostate cancer. PloS one 2010, 5(5):e10547. 10.1371/journal.pone.0010547, 2866657, 20479932.
26. Paoloni-Giacobino A, Chen H, Peitsch MC, Rossier C, Antonarakis SE. Cloning of the TMPRSS2 gene, which encodes a novel serine protease with transmembrane, LDLRA, and SRCR domains and maps to 21q22.3. Genomics 1997, 44(3):309-320. 10.1006/geno.1997.4845, 9325052.
27. Rao VN, Papas TS, Reddy ES. erg, a human ets-related gene on chromosome 21: alternative splicing, polyadenylation, and translation. Science 1987, 237(4815):635-639. 10.1126/science.3299708, 3299708.
28. Owczarek CM, Portbury KJ, Hardy MP, O'Leary DA, Kudoh J, Shibuya K, Shimizu N, Kola I, Hertzog PJ. Detailed mapping of the ERG-ETS2 interval of human chromosome 21 and comparison with the region of conserved synteny on mouse chromosome 16. Gene 2004, 324:65-77.
29. Hu Y, Dobi A, Sreenath T, Cook C, Tadase AY, Ravindranath L, Cullen J, Furusato B, Chen Y, Thangapazham RL, et al. Delineation of TMPRSS2-ERG splice variants in prostate cancer. Clin cancer Res: an Off J of the Am Assoc for Cancer Res 2008, 14(15):4719-4725.
30. Wang Q, Li W, Liu XS, Carroll JS, Janne OA, Keeton EK, Chinnaiyan AM, Pienta KJ, Brown M. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol cell 2007, 27(3):380-392. 10.1016/j.molcel.2007.05.041, 17679089.
31. Werner T. The promoter connection. Nat Genet 2001, 29(2):105-106. 10.1038/ng1001-105, 11586286.
32. McMullin RP, Dobi A, Mutton LN, Orosz A, Maheshwari S, Shashikant CS, Bieberich CJ. A FOXA1-binding enhancer regulates Hoxb13 expression in the prostate gland. Proc Natl Acad Sci USA 2010, 107(1):98-103. 10.1073/pnas.0902001107, 2806740, 20018680.
33. Zhan M. Deciphering modular and dynamic behaviors of transcriptional networks. Genomic Med 2007, 1(1-2):19-28. 2276884, 18923925.
34. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21(13):2933-2942. 10.1093/bioinformatics/bti473, 15860560.
35. Masuda K, Werner T, Maheshwari S, Frisch M, Oh S, Petrovics G, May K, Srikantan V, Srivastava S, Dobi A. Androgen receptor binding sites identified by a GREF_GATA model. J of mMol Biol 2005, 353(4):763-771.
36. Spitz F, Furlong EE. Transcription factors: from enhancer binding to developmental control. Nature reviews Genetics 2012, 13(9):613-626. 10.1038/nrg3207, 22868264.
37. Hihnala S, Kujala M, Toppari J, Kere J, Holmberg C, Hoglund P. Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea. Mol human Reprod 2006, 12(2):107-111.
38. Tan PY, Chang CW, Chng KR, Wansa KD, Sung WK, Cheung E. Integration of regulatory networks by NKX3-1 promotes androgen-dependent prostate cancer survival. Mol and cell Biol 2012, 32(2):399-414.
39. Burkhardt L, Fuchs S, Krohn A, Masser S, Mader M, Kluth M, Bachmann F, Huland H, Steuber T, Graefen M, et al. CHD1 is a 5q21 tumor suppressor required for ERG rearrangement in prostate cancer. Cancer Res 2013, 73(9):2795-2805. 10.1158/0008-5472.CAN-12-1342, 23492366.
40. Lei Q, Jiao J, Xin L, Chang CJ, Wang S, Gao J, Gleave ME, Witte ON, Liu X, Wu H. NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer cell 2006, 9(5):367-378. 10.1016/j.ccr.2006.03.031, 16697957.
41. Song LN, Bowen C, Gelmann EP. Structural and functional interactions of the prostate cancer suppressor protein NKX3.1 with topoisomerase I. The Biochem J 2013, 453(1):125-136.
42. Eide T, Ramberg H, Glackin C, Tindall D, Tasken KA. TWIST1, A novel androgen-regulated gene, is a target for NKX3-1 in prostate cancer cells. Cancer cell Int 2013, 13(1):4. 10.1186/1475-2867-13-4, 3626792, 23368843.
43. Vij N, Mazur S, Zeitlin PL. CFTR is a negative regulator of NFkappaB mediated innate immune response. PloS one 2009, 4(2):e4664. 10.1371/journal.pone.0004664, 2647738, 19247502.
44. Markowski MC, Bowen C, Gelmann EP. Inflammatory cytokines induce phosphorylation and ubiquitination of prostate suppressor protein NKX3.1. Cancer Res 2008, 68(17):6896-6901. 10.1158/0008-5472.CAN-08-0578, 2586101, 18757402.
45. Shinohara DB, Vaghasia AM, Yu SH, Mak TN, Bruggemann H, Nelson WG, De Marzo AM, Yegnasubramanian S, Sfanos KS. A mouse model of chronic prostatic inflammation using a human prostate cancer-derived isolate of Propionibacterium acnes. Prostate 2013, 73(9):1007-1015. 10.1002/pros.22648, 23389852.
46. Debelec-Butuner B, Alapinar C, Varisli L, Erbaykent-Tepedelen B, Hamid SM, Gonen-Korkmaz C, Korkmaz KS. Inflammation-mediated abrogation of androgen signaling: an in vitro model of prostate cell inflammation. Mol Carcinog 2012 Aug 21, doi:10.1002/mc.21948.
47. Khalili M, Mutton LN, Gurel B, Hicks JL, De Marzo AM, Bieberich CJ. Loss of Nkx3.1 expression in bacterial prostatitis: a potential link between inflammation and neoplasia. The Am Jof pathology 2010, 176(5):2259-2268.
48. Mohamed AA, Tan SH, Sun C, Shaheduzzaman S, Hu Y, Petrovics G, Chen Y, Sesterhenn IA, Li H, Sreenath T, et al. ERG oncogene modulates prostaglandin signaling in prostate cancer cells. Cancer Biol & therapy 2011, 11(4):410-417.
49. Petrovics G, Liu A, Shaheduzzaman S, Furusato B, Sun C, Chen Y, Nau M, Ravindranath L, Dobi A, Srikantan V, et al. Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene 2005, 24(23):3847-3852. 10.1038/sj.onc.1208518, 15750627.
50. Mwamukonda K, Chen Y, Ravindranath L, Furusato B, Hu Y, Sterbis J, Osborn D, Rosner I, Sesterhenn IA, McLeod DG, et al. Quantitative expression of TMPRSS2 transcript in prostate tumor cells reflects TMPRSS2-ERG fusion status. Prostate cancer and prostatic Dis 2010, 13(1):47-51.
51. Richter E, Masuda K, Cook C, Ehrich M, Tadese AY, Li H, Owusu A, Srivastava S, Dobi A. A role for DNA methylation in regulating the growth suppressor PMEPA1 gene in prostate cancer. Epigenetics: Off J of the DNA Methylation Soc 2007, 2(2):100-109.