Targeted radiosensitization of ETS fusion-positive prostate cancer through PARP1 inhibition

Neoplasia (United States)

Volumn 15, Issue 10, 2013, Pages 1207-1217

  Han, Sumin ^a   Brenner, J Chad ^a   Sabolch, Aaron ^a   Jackson, Will ^a   Speers, Corey ^a   Wilder Romans, Kari ^a   Knudsen, Karen E ^b,c   Lawrence, Theodore S ^a   Chinnaiyan, Arul M ^a,b   Feng, Felix Y ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; TRANSCRIPTION FACTOR ERG; VELIPARIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; COMET ASSAY; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; ERG GENE; ETS GENE; FLOW CYTOMETRY; GENE; GENE FUSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IRRADIATION; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; RADIOSENSITIVITY; RADIOSENSITIZATION; TUMOR VOLUME; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; DNA REPAIR; GENE FUSION; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, SCID; PHTHALAZINES; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASES; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-ETS; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; TRANS-ACTIVATORS;

EID: 84887054899     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.131604     Document Type: Article

References (56)

1. Kumar-Sinha C, Tomlins SA, and Chinnaiyan AM (2008). Recurrent gene fusions in prostate cancer. Nat Rev Cancer 8, 497-511.
2. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, et al. (2005). Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310, 644-648.
3. Brenner JC and Chinnaiyan AM (2009). Translocations in epithelial cancers. Biochim Biophys Acta 1796, 201-215.
4. Lapointe J, Kim YH, Miller MA, Li C, Kaygusuz G, van de Rijn M, Huntsman DG, Brooks JD, and Pollack JR (2007). A variant TMPRSS2 isoform and ERG fusion product in prostate cancer with implications for molecular diagnosis. Mod Pathol 20, 467-473.
5. Mehra R, Tomlins SA, Shen R, Nadeem O, Wang L, Wei JT, Pienta KJ, Ghosh D, Rubin MA, Chinnaiyan AM, et al. (2007). Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer. Mod Pathol 20, 538-544.
6. Mosquera JM, Perner S, Demichelis F, Kim R, Hofer MD, Mertz KD, Paris PL, Simko J, Collins C, Bismar TA, et al. (2007). Morphological features of TMPRSS2-ERG gene fusion prostate cancer. J Pathol 212, 91-101.
7. Soller MJ, Isaksson M, Elfving P, Soller W, Lundgren R, and Panagopoulos I (2006). Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer. Genes Chromosomes Cancer 45, 717-719.
8. Tognon C, Knezevich SR, Huntsman D, Roskelley CD, Melnyk N, Mathers JA, Becker L, Carneiro F, MacPherson N, Horsman D, et al. (2002). Expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell 2, 367-376.
9. Oh S, Shin S, and Janknecht R (2012). ETV1, 4 and 5: an oncogenic subfamily of ETS transcription factors. Biochim Biophys Acta 1826, 1-12.
10. Fuka G, Kauer M, Kofler R, Haas OA, and Panzer-Grumayer R (2011). The leukemia-specific fusion gene ETV6/RUNX1 perturbs distinct key biological functions primarily by gene repression. PLoS One 6, e26348.
11. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, Alimonti A, Nardella C, Varmeh S, Scardino PT, et al. (2009). Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 41, 619-624.
12. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH, Taylor BS, Sander C, Cardiff RD, Couto SS, et al. (2009). Cooperativity of TMPRSS2- ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 41, 524-526.
13. Klezovitch O, Risk M, Coleman I, Lucas JM, Null M, True LD, Nelson PS, and Vasioukhin V (2008). A causal role for ERG in neoplastic transformation of prostate epithelium. Proc Natl Acad Sci USA 105, 2105-2110.
14. Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, Helgeson BE, Cao Q, Prensner JR, Rubin MA, Shah RB, et al. (2008). Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 10, 177-188.
15. Brenner JC, Ateeq B, Li Y, Yocum AK, Cao Q, Asangani IA, Patel S, Wang X, Liang H, Yu J, et al. (2011). Mechanistic rationale for inhibition of poly(ADP-ribose) polymerase in ETS gene fusion-positive prostate cancer. Cancer Cell 19, 664-678.
16. Dantzer F, de La Rubia G, Ménissier-De Murcia J, Hostomsky Z, de Murcia G, and Schreiber V (2000). Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry 39, 7559-7569.
17. Dantzer F, Schreiber V, Niedergang C, Trucco C, Flatter E, De La Rubia G, Oliver J, Rolli V, Ménissier-de Murcia J, and de Murcia G (1999). Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie 81, 69-75.
18. Bryant HE and Helleday T (2006). Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res 34, 1685-1691.
19. Hegan DC, Lu Y, Stachelek GC, Crosby ME, Bindra RS, and Glazer PM (2010). Inhibition of poly(ADP-ribose) polymerase down-regulates BRCA1 and RAD51 in a pathway mediated by E2F4 and p130. Proc Natl Acad Sci USA 107, 2201-2206.
20. Saberi A, Hochegger H, Szuts D, Lan L, Yasui A, Sale JE, Taniguchi Y, Murakawa Y, Zeng W, Yokomori K, et al. (2007). RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination- mediated repair. Mol Cell Biol 27, 2562-2571.
21. Mitchell J, Smith GC, and Curtin NJ (2009). Poly(ADP-ribose) polymerase-1 and DNA-dependent protein kinase have equivalent roles in double strand break repair following ionizing radiation. Int J Radiat Oncol Biol Phys 75, 1520-1527.
22. Nowsheen S, Bonner JA, and Yang ES (2011). The poly(ADP-ribose) polymer-ase inhibitor ABT-888 reduces radiation-induced nuclear EGFR and augments head and neck tumor response to radiotherapy. Radiother Oncol 99, 331-338.
23. Wang M, Wu W, Rosidi B, Zhang L, Wang H, and Iliakis G (2006). PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34, 6170-6182.
24. Schiewer MJ, Goodwin JF, Han S, Brenner JC, Augello MA, Dean JL, Liu F, Planck JL, Ravindranathan P, Chinnaiyan AM, et al. (2012). Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov 2, 1134-1149.
25. D'Amours D, Desnoyers S, D'Silva I, and Poirier GG (1999). Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342(pt 2), 249-268.
26. Kim MY, Zhang T, and Kraus WL (2005). Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 19, 1951-1967.
27. Feng FY, Blas K, Olson K, Stenmark M, Sandler H, and Hamstra DA (2013). Retrospective evaluation reveals that long-term androgen deprivation therapy improves cause-specific and overall survival in the setting of dose-escalated radiation for high-risk prostate cancer. Int J Radiat Oncol Biol Phys 86, 64-71.
28. Brenner JC, Graham MP, Kumar B, Saunders LM, Kupfer R, Lyons RH, Bradford CR, and Carey TE (2009). Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines. Head Neck 32, 417-426.
29. Fertil B, Dertinger H, Courdi A, and Malaise EP (1984). Mean inactivation dose: a useful concept for intercomparison of human cell survival curves. Radiat Res 99, 73-84.
30. Ferro AM and Olivera BM (1982). Poly(ADP-ribosylation) in vitro. Reaction parameters and enzyme mechanism. J Biol Chem 257, 7808-7813.
31. Caldecott KW (2003). XRCC1 and DNA strand break repair. DNA Repair (Amst) 2, 955-969.
32. Attard G, Clark J, Ambroisine L, Fisher G, Kovacs G, Flohr P, Berney D, Foster CS, Fletcher A, Gerald WL, et al. (2008). Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene 27, 253-263.
33. Demichelis F, Fall K, Perner S, Andrén O, Schmidt F, Setlur SR, Hoshida Y, Mosquera JM, Pawitan Y, Lee C, et al. (2007). TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene 26, 4596-4599.
34. Nam RK, Sugar L, Yang W, Srivastava S, Klotz LH, Yang LY, Stanimirovic A, Encioiu E, Neill M, Loblaw DA, et al. (2007). Expression of the TMPRSS2: ERG fusion gene predicts cancer recurrence after surgery for localised prostate cancer. Br J Cancer 97, 1690-1695.
35. Perner S, Rupp NJ, Braun M, Rubin MA, Moch H, Dietel M, Wernert N, Jung K, Stephan C, and Kristiansen G (2013). 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, 807-812.
36. Wang J, Cai Y, Ren C, and Ittmann M (2006). Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res 66, 8347-8351.
37. Perner S, Svensson MA, Hossain RR, Day JR, Groskopf J, Slaughter RC, Jarleborn AR, Hofer MD, Kuefer R, Demichelis F, et al. (2010). ERG rearrangement metastasis patterns in locally advanced prostate cancer. Urology 75, 762-767.
38. Gopalan A, Leversha MA, Satagopan JM, Zhou Q, Al-Ahmadie HA, Fine SW, Eastham JA, Scardino PT, Scher HI, Tickoo SK, et al. (2009). TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy. Cancer Res 69, 1400-1406.
39. Hoogland AM, Jenster G, van Weerden WM, Trapman J, van der Kwast T, Roobol MJ, Schroder FH, Wildhagen MF, and van Leenders GJ (2012). ERG immunohistochemistry is not predictive for PSA recurrence, local recurrence or overall survival after radical prostatectomy for prostate cancer. Mod Pathol 25, 471-479.
40. Minner S, Enodien M, Sirma H, Luebke AM, Krohn A, Mayer PS, Simon R, Tennstedt P, Muller J, Scholz L, et al. (2011). ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy. Clin Cancer Res 17, 5878-5888.
41. Toubaji A, Albadine R, Meeker AK, Isaacs WB, Lotan T, Haffner MC, Chaux A, Epstein JI, Han M, Walsh PC, et al. (2011). Increased gene copy number of ERG on chromosome 21 but not TMPRSS2-ERG fusion predicts outcome in prostatic adenocarcinomas. Mod Pathol 24, 1511-1520.
42. Säramaki OR, Harjula AE, Martikainen PM, Vessella RL, Tammela TL, and Visakorpi T (2008). TMPRSS2:ERG fusion identifies a subgroup of prostate cancers with a favorable prognosis. Clin Cancer Res 14, 3395-3400.
43. Petrovics G, Liu A, Shaheduzzaman S, Furusato B, Sun C, Chen Y, Nau M, Ravindranath L, Dobi A, Srikantan V, et al. (2005). Frequent overexpression of ETS-related gene-1 (ERG1) in prostate cancer transcriptome. Oncogene 24, 3847-3852.
44. Chen Y, Chi P, Rockowitz S, Iaquinta PJ, Shamu T, Shukla S, Gao D, Sirota I, Carver BS, Wongvipat J, et al. (2013). ETS factors reprogram the androgen receptor cistrome and prime prostate tumorigenesis in response to PTEN loss. Nat Med 19, 1023-1029.
45. Yu J, Mani RS, Cao Q, Brenner CJ, Cao X, Wang X, Wu L, Li J, Hu M, Gong Y, et al. (2010). An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17, 443-454.
46. Swanson TA, Krueger SA, Galoforo S, Thibodeau BJ, Martinez AA, Wilson GD, and Marples B (2011). TMPRSS2/ERG fusion gene expression alters chemo- and radio-responsiveness in cell culture models of androgen independent prostate cancer. Prostate 71, 1548-1558.
47. Debes JD and Tindall DJ (2002). The role of androgens and the androgen receptor in prostate cancer. Cancer Lett 187, 1-7.
48. Horwitz EM, Bae K, Hanks GE, Porter A, Grignon DJ, Brereton HD, Venkatesan V, Lawton CA, Rosenthal SA, Sandler HM, et al. (2008). Ten-year follow-up of radiation therapy oncology group protocol 92-02: a phase III trial of the duration of elective androgen deprivation in locally advanced prostate cancer. J Clin Oncol 26, 2497-2504.
49. Lawton CA, Winter K, Murray K, Machtay M, Mesic JB, Hanks GE, Coughlin CT, and Pilepich MV (2001). Updated results of the phase III Radiation Therapy Oncology Group (RTOG) trial 85-31 evaluating the potential benefit of androgen suppression following standard radiation therapy for unfavor- able prognosis carcinoma of the prostate. Int J Radiat Oncol Biol Phys 49, 937-946.
50. Wu D, Zhang C, Shen Y, Nephew KP, and Wang Q (2011). Androgen receptor-driven chromatin looping in prostate cancer. Trends Endocrinol Metab 22, 474-480.
51. Bastus NC, Boyd LK, Mao X, Stankiewicz E, Kudahetti SC, Oliver RT, Berney DM, and Lu YJ (2010). Androgen-induced TMPRSS2:ERG fusion in non- malignant prostate epithelial cells. Cancer Res 70, 9544-9548.
52. Mani RS, Tomlins SA, Callahan K, Ghosh A, Nyati MK, Varambally S, Palanisamy N, and Chinnaiyan AM (2009). Induced chromosomal proximity and gene fusions in prostate cancer. Science 326, 1230.
53. Chatterjee P, Choudhary GS, Sharma A, Singh K, Heston WD, Ciezki J, Klein EA, and Almasan A (2013). PARP inhibition sensitizes to low dose-rate radiation TMPRSS2-ERG fusion gene-expressing and PTEN-deficient prostate cancer cells. PLoS One 8, e60408.
54. Lee HJ, Yoon C, Schmidt B, Park DJ, Zhang AY, Erkizan HV, Toretsky JA, Kirsch DG, and Yoon SS (2013). Combining poly(ADP-ribose) polymerase 1 (PARP-1) inhibition and radiation in Ewings sarcoma results in lethal DNA damage. Mol Cancer Ther, E-pub ahead of print.
55. Brenner JC, Feng FY, Han S, Patel S, Goyal SV, Bou-Maroun LM, Liu M, Lonigro R, Prensner JR, Tomlins SA, et al. (2012). PARP-1 inhibition as a targeted strategy to treat Ewing's sarcoma. Cancer Res 72, 1608-1613.
56. Tomlins SA, Aubin SM, Siddiqui J, Lonigro RJ, Sefton-Miller L, Miick S, Williamsen S, Hodge P, Meinke J, Blase A, et al. (2011). Urine TMPRSS2: ERG fusion transcript stratifies prostate cancer risk in men with elevated serum PSA. Sci Transl Med 3, 94ra72.