PIAS1 is a crucial factor for prostate cancer cell survival and a valid target in docetaxel resistant cells

Oncotarget

Volumn 5, Issue 23, 2014, Pages 12043-12056

  Puhr, Martin ^a   Hoefer, Julia ^a   Neuwirt, Hannes ^a   Eder, Iris E ^a   Kern, Johann ^b   Schäfer, Georg ^a   Geley, Stephan ^a   Heidegger, Isabel ^a   Klocker, Helmut ^a   Culig, Zoran ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b Tumor Biology and Angiogenesis Laboratory   (Austria)

Author keywords

Apoptosis; Chemotherapy resistance; Docetaxel; PIAS1; Prostate cancer

Indexed keywords

PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN INHIBITOR OF ACTIVATED STAT 1; PROTEIN MCL 1; PROTEIN P21; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; DOCETAXEL; PIAS1 PROTEIN, HUMAN; SMALL INTERFERING RNA; SUMO PROTEIN; TAXOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL SURVIVAL; CHICKEN; CHORIOALLANTOIS; CONTROLLED STUDY; DRUG TARGETING; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR XENOGRAFT; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; DRUG RESISTANCE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; PROSTATE TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; PROSTATIC NEOPLASMS; PROTEIN INHIBITORS OF ACTIVATED STAT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TAXOIDS; TISSUE ARRAY ANALYSIS; TRANSFECTION;

EID: 84920024628     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2658     Document Type: Article

References (50)

1. Saad F, Ruether D, Ernst S, North S, Cheng T, Perrotte P, Karakiewicz P, Winquist E. The Canadian Uro-Oncology Group multicentre phase II study of docetaxel administered every 3 weeks with prednisone in men with metastatic hormone-refractory prostate cancer progressing after mitoxantrone/ prednisone. BJU international. 2008; 102:551-555.
2. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Theodore C, James ND, Turesson I, Rosenthal MA, Eisenberger MA. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. The New England journal of medicine. 2004; 351:1502-1512.
3. Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr, Jones JA, Taplin ME, Burch PA, Berry D, Moinpour C, Kohli M, Benson MC, Small EJ, Raghavan D, Crawford ED. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. The New England journal of medicine. 2004; 351:1513-1520.
4. Geney R, Ungureanu LM, Li D, Ojima I. Overcoming multidrug resistance in taxane chemotherapy. Clinical chemistry and laboratory medicine: CCLM / FESCC 2002; 40:918-925.
5. Armstrong AJ, Garrett-Mayer E, de Wit R, Tannock I, Eisenberger M. Prediction of survival following first-line chemotherapy in men with castration-resistant metastatic prostate cancer. Clin Cancer Res. 2010; 16:203-211.
6. Murray S, Briasoulis E, Linardou H, Bafaloukos D, Papadi-mitriou C. Taxane resistance in breast cancer: mechanisms, predictive biomarkers and circumvention strategies. Cancer Treat Rev. 2012; 38:890-903.
7. Mahon KL, Henshall SM, Sutherland RL, Horvath LG. Pathways of chemotherapy resistance in castration-resistant prostate cancer. Endocr Relat Cancer. 2011; 18:R103-123.
8. Ploussard G, Terry S, Maille P, Allory Y, Sirab N, Kheuang L, Soyeux P, Nicolaiew N, Coppolani E, Paule B, Salomon L, Culine S, Buttyan R, Vacherot F, de la Taille A. Class III beta-tubulin expression predicts prostate tumor aggressiveness and patient response to docetaxel-based chemotherapy. Cancer Res. 2010; 70:9253-9264.
9. Terry S, Ploussard G, Allory Y, Nicolaiew N, Boissiere-Michot F, Maille P, Kheuang L, Coppolani E, Ali A, Bibeau F, Culine S, Buttyan R, de la Taille A, Vacherot F. Increased expression of class III beta-tubulin in castration-resistant human prostate cancer. Br J Cancer. 2009; 101:951-956.
10. Sanchez C, Mendoza P, Contreras HR, Vergara J, McCubrey JA, Huidobro C, Castellon EA. Expression of multidrug resistance proteins in prostate cancer is related with cell sensitivity to chemotherapeutic drugs. Prostate. 2009; 69:1448-1459.
11. Lee JT Jr, Steelman LS, McCubrey JA. Phosphatidylinositol 3'-kinase activation leads to multidrug resistance protein-1 expression and subsequent chemoresistance in advanced prostate cancer cells. Cancer Res. 2004; 64:8397-8404.
12. Arai T, Miyoshi Y, Kim SJ, Akazawa K, Maruyama N, Taguchi T, Tamaki Y, Noguchi S. Association of GSTP1 expression with resistance to docetaxel and paclitaxel in human breast cancers. Eur J Surg Oncol. 2008; 34:734-738.
13. Rahman KM, Banerjee S, Ali S, Ahmad A, Wang Z, Kong D, Sakr WA. 3, 3'-Diindolylmethane enhances taxotereinduced apoptosis in hormone-refractory prostate cancer cells through survivin down-regulation. Cancer Res. 2009; 69:4468-4475.
14. Ling X, Cao S, Cheng Q, Keefe JT, Rustum YM, Li F. A novel small molecule FL118 that selectively inhibits survivin, Mcl-1, XIAP, and cIAP2 in a p53-independent manner, shows superior antitumor activity. PLoS One. 2012; 7:e45571.
15. Hayashi N, Asano K, Suzuki H, Yamamoto T, Tanigawa N, Egawa S, Manome Y. Adenoviral infection of survivin antisense sensitizes prostate cancer cells to etoposide in vivo. Prostate. 2005; 65:10-19.
16. Yoshino T, Shiina H, Urakami S, Kikuno N, Yoneda T, Shigeno K, Igawa M. Bcl-2 expression as a predictive marker of hormone-refractory prostate cancer treated with taxane-based chemotherapy. Clin Cancer Res. 2006; 12:6116-6124.
17. Vilenchik M, Raffo AJ, Benimetskaya L, Shames D, Stein CA. Antisense RNA down-regulation of bcl-xL Expression in prostate cancer cells leads to diminished rates of cellular proliferation and resistance to cytotoxic chemotherapeutic agents. Cancer Res. 2002; 62:2175-2183.
18. Sjostrom J, Blomqvist C, von Boguslawski K, Bengtsson NO, Mjaaland I, Malmstrom P, Ostenstadt B, Wist E, Valvere V, Takayama S, Reed JC, Saksela E. The predictive value of bcl-2, bax, bcl-xL, bag-1, fas, and fasL for chemotherapy response in advanced breast cancer. Clin Cancer Res. 2002; 8:811-816.
19. Morris MJ, Cordon-Cardo C, Kelly WK, Slovin SF, Siedlecki K, Regan KP, DiPaola RS, Rafi M, Rosen N, Scher HI. Safety and biologic activity of intravenous BCL-2 antisense oligonucleotide (G3139) and taxane chemotherapy in patients with advanced cancer. Appl Immunohistochem Mol Morphol. 2005; 13:6-13.
20. Tolcher AW, Kuhn J, Schwartz G, Patnaik A, Hammond LA, Thompson I, Fingert H, Bushnell D, Malik S, Kreisberg J, Izbicka E, Smetzer L, Rowinsky EK. A Phase I pharmacokinetic and biological correlative study of oblimersen sodium (genasense, g3139), an antisense oligonucleotide to the bcl-2 mRNA, and of docetaxel in patients with hormone-refractory prostate cancer. Clin Cancer Res. 2004; 10:5048-5057.
21. Satoh T, Okamoto I, Miyazaki M, Morinaga R, Tsuya A, Hasegawa Y, Terashima M, Ueda S, Fukuoka M, Ariyoshi Y, Saito T, Masuda N, Watanabe H, Taguchi T, Kakihara T, Aoyama Y, et al. Phase I study of YM155, a novel survivin suppressant, in patients with advanced solid tumors. Clin Cancer Res. 2009; 15:3872-3880.
22. Dean E, Jodrell D, Connolly K, Danson S, Jolivet J, Durkin J, Morris S, Jowle D, Ward T, Cummings J, Dickinson G, Aarons L, Lacasse E, Robson L, Dive C, Ranson M. Phase I trial of AEG35156 administered as a 7-day and 3-day continuous intravenous infusion in patients with advanced refractory cancer. J Clin Oncol. 2009; 27:1660-1666.
23. Sharrocks AD. PIAS proteins and transcriptional regulation-more than just SUMO E3 ligases? Genes Dev. 2006; 20:754-758.
24. Liu B, Liao J, Rao X, Kushner SA, Chung CD, Chang DD, Shuai K. Inhibition of Stat1-mediated gene activation by PIAS1. Proc Natl Acad Sci USA. 1998; 95:10626-10631.
25. Chung CD, Liao J, Liu B, Rao X, Jay P, Berta P, Shuai K. Specific inhibition of Stat3 signal transduction by PIAS3. Science. 1997; 278:1803-1805.
26. Domingo-Domenech J, Oliva C, Rovira A, Codony-Servat J, Bosch M, Filella X, Montagut C, Tapia M, Campas C, Dang L, Rolfe M, Ross JS, Gascon P, Albanell J, Mellado B. Interleukin 6, a nuclear factor-kappaB target, predicts resistance to docetaxel in hormone-independent prostate cancer and nuclear factor-kappaB inhibition by PS-1145 enhances docetaxel antitumor activity. Clin Cancer Res. 2006; 12:5578-5586.
27. Codony-Servat J, Marin-Aguilera M, Visa L, Garcia-Albeniz X, Pineda E, Fernandez PL, Filella X, Gascon P, Mellado B. Nuclear factor-kappaB and interleukin-6 related docetaxel resistance in castrationresistant prostate cancer. Prostate. 2013; 73:512-521.
28. Shima H, Suzuki H, Sun J, Kono K, Shi L, Kinomura A, Horikoshi Y, Ikura T, Ikura M, Kanaar R, Igarashi K, Saitoh H, Kurumizaka H, Tashiro S. Activation of the SUMO modification system is required for the accumulation of RAD51 at sites of DNA damage. J Cell Sci. 2013; 126:5284-5292.
29. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature. 2009; 462:935-939.
30. Kahyo T, Nishida T, Yasuda H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol Cell. 2001; 8:713-718.
31. Munarriz E, Barcaroli D, Stephanou A, Townsend PA, Maisse C, Terrinoni A, Neale MH, Martin SJ, Latchman DS, Knight RA, Melino G, De Laurenzi V. PIAS-1 is a checkpoint regulator which affects exit from G1 and G2 by sumoylation of p73. Mol Cell Biol. 2004; 24:10593-10610.
32. Schmidt D, Muller S. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci USA. 2002; 99:2872-2877.
33. Hoefer J, Schafer G, Klocker H, Erb HH, Mills IG, Hengst L, Puhr M, Culig Z. PIAS1 is increased in human prostate cancer and enhances proliferation through inhibition of p21. Am J Pathol. 2012; 180:2097-2107.
34. Puhr M, Hoefer J, Schafer G, Erb HH, Oh SJ, Klocker H, Heidegger I, Neuwirt H, Culig Z. Epithelial-to-mesenchymal transition leads to docetaxel resistance in prostate cancer and is mediated by reduced expression of miR-200c and miR-205. Am J Pathol. 2012; 181:2188-2201.
35. Coppola D, Parikh V, Boulware D, Blanck G. Substantially reduced expression of PIAS1 is associated with colon cancer development. J Cancer Res Clin Oncol. 2009; 135:1287-1291.
36. Brantley EC, Nabors LB, Gillespie GY, Choi YH, Palmer CA, Harrison K, Roarty K, Benveniste EN. Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression. Clin Cancer Res. 2008; 14:4694-4704.
37. Li P, Yu X, Ge K, Melamed J, Roeder RG, Wang Z. Heterogeneous expression and functions of androgen receptor co-factors in primary prostate cancer. Am J Pathol. 2002; 161:1467-1474.
38. Gross M, Liu B, Tan J, French FS, Carey M, Shuai K. Distinct effects of PIAS proteins on androgen-mediated gene activation in prostate cancer cells. Oncogene. 2001; 20:3880-3887.
39. Heemers HV, Regan KM, Schmidt LJ, Anderson SK, Ballman KV, Tindall DJ. Androgen modulation of coregulator expression in prostate cancer cells. Mol Endocrinol. 2009; 23:572-583.
40. Stephanou A, Latchman DS. STAT-1: a novel regulator of apoptosis. Int J Exp Pathol. 2003; 84:239-244.
41. Patterson SG, Wei S, Chen X, Sallman DA, Gilvary DL, Zhong B, Pow-Sang J, Yeatman T, Djeu JY. Novel role of Stat1 in the development of docetaxel resistance in prostate tumor cells. Oncogene. 2006; 25:6113-6122.
42. Nozell S, Chen X. p21B, a variant of p21(Waf1/Cip1), is induced by the p53 family. Oncogene. 2002; 21:1285-1294.
43. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K, Kitada S, Reed JC. Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol. 1996; 148:1567-1576.
44. Zhang S, Zhau HE, Osunkoya AO, Iqbal S, Yang X, Fan S, Chen Z, Wang R, Marshall FF, Chung LW, Wu D. Vascular endothelial growth factor regulates myeloid cell leukemia-1 expression through neuropilin-1-dependent activation of c-MET signaling in human prostate cancer cells. Mol Cancer. 2010; 9:9.
45. Cavarretta IT, Neuwirt H, Untergasser G, Moser PL, Zaki MH, Steiner H, Rumpold H, Fuchs D, Hobisch A, Nemeth JA, Culig Z. The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene. 2007; 26:2822-2832.
46. Liu G, Kelly WK, Wilding G, Leopold L, Brill K, Somer B. An open-label, multicenter, phase I/II study of single-agent AT-101 in men with castrate-resistant prostate cancer. Clin Cancer Res. 2009; 15:3172-3176.
47. Sonpavde G, Matveev V, Burke JM, Caton JR, Fleming MT, Hutson TE, Galsky MD, Berry WR, Karlov P, Holmlund JT, Wood BA, Brookes M, Leopold L. Randomized phase II trial of docetaxel plus prednisone in combination with placebo or AT-101, an oral small molecule Bcl-2 family antagonist, as first-line therapy for metastatic castrationresistant prostate cancer. Ann Oncol. 2012; 23:1803-1808.
48. Puhr M, Santer FR, Neuwirt H, Susani M, Nemeth JA, Hobisch A, Kenner L, Culig Z. Down-regulation of suppressor of cytokine signaling-3 causes prostate cancer cell death through activation of the extrinsic and intrinsic apoptosis pathways. Cancer Res. 2009; 69:7375-7384.
49. Sigl R, Wandke C, Rauch V, Kirk J, Hunt T, Geley S. Loss of the mammalian APC/C activator FZR1 shortens G1 and lengthens S phase but has little effect on exit from mitosis. J Cell Sci. 2009; 122:4208-4217.
50. Deryugina EI, Quigley JP. Chapter 2. Chick embryo chorioallantoic membrane models to quantify angiogenesis induced by inflammatory and tumor cells or purified effector molecules. Methods Enzymol. 2008; 444:21-41.