Differential targeting of androgen and glucocorticoid receptors induces ER stress and apoptosis in prostate cancer cells: A novel therapeutic modality

Cell Cycle

Volumn 11, Issue 2, 2012, Pages 395-406

  Yemelyanov, Alexander ^a   Bhalla, Pankaj ^a   Yang, Ximing ^a   Ugolkov, Andrey ^b   Iwadate, Kenichi ^c   Karseladze, Apollon ^d   Budunova, Irina ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Northwestern University   (United States)

^d N N BLOKHIN RUSSIAN CANCER RESEARCH CENTER   (Russian Federation)

Author keywords

Apoptosis; ER stress; Non steroidal modulator; Prostate cancer; Proteasome inhibitor

Indexed keywords

2 (4 ACETOXYPHENYL) 2 CHLORO N METHYLETHYLAMMONIUM CHLORIDE; ANDROGEN RECEPTOR; BICALUTAMIDE; BORTEZOMIB; CCAAT ENHANCER BINDING PROTEIN; DEXAMETHASONE; DOCETAXEL; FLUTAMIDE; GLUCOCORTICOID RECEPTOR; INTERLEUKIN 1; LENTIVIRUS VECTOR; PROTEASOME INHIBITOR; SHORT HAIRPIN RNA; STEROID RECEPTOR; UNCLASSIFIED DRUG;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER INHIBITION; CARCINOGENESIS; CELL GROWTH; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG TARGETING; ENDOPLASMIC RETICULUM STRESS; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; ONCOGENE; PROSTATE CANCER; PROSTATECTOMY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84862965339     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.2.18945     Document Type: Article

References (50)

1. Dehm SM, Tindall DJ. Molecular regulation of androgen action in prostate cancer. J Cell Biochem 2006; 99:333-44; PMID:16518832; http://dx.doi.org/10. 1002/jcb.20794.
2. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001; 1:34-45; PMID:11900250; http://dx.doi.org/10.1038/ 35094009.
3. Heinlein CA, Chang C. Androgen receptor in prostate cancer. Endocr Rev 2004; 25:276-308; PMID:15082523; http://dx.doi.org/10.1210/er.2002-0032.
4. Singh P, Uzgare A, Litvinov I, Denmeade SR, Isaacs JT. Combinatorial androgen receptor targeted therapy for prostate cancer. Endocr Relat Cancer 2006; 13:653-66; PMID:16954423; http://dx.doi.org/10.1677/erc.1.00797.
5. Dondi D, Maggi R, Scaccianoce E, Martini L, Motta M, Poletti A. Expression and role of functional glucocorticoid receptors in the human androgen-independent prostate cancer cell line, DU145. J Mol Endocrinol 2001; 26:185-91; PMID:11357055; http://dx.doi.org/10.1677/jme.0.0260185.
6. Smith RG, Syms AJ, Nag A, Lerner S, Norris JS. Mechanism of the glucocorticoid regulation of growth of the androgen-sensitive prostate-derived R3327HG8-A1 tumor cell line. J Biol Chem 1985; 260:12454-63; PMID:3876336.
7. Nishimura K, Nonomura N, Satoh E, Harada Y, Nakayama M, Tokizane T, et al. Potential mechanism for the effects of dexamethasone on growth of androgen-independent prostate cancer. J Natl Cancer Inst 2001; 93:1739-46; PMID:11717335; http://dx.doi.org/10.1093/jnci/93.22.1739.
8. Yano A, Fujii Y, Iwai A, Kawakami S, Kageyama Y, Kihara K. Glucocorticoids suppress tumor lymphangiogenesis of prostate cancer cells. Clin Cancer Res 2006; 12:6012-7; PMID:17062674; http://dx.doi.org/10.1158/1078-0432. CCR-06-0749.
9. Yemelyanov A, Czwornog J, Chebotaev D, Karseladze A, Kulevitch E, Yang X, et al. Tumor suppressor activity of glucocorticoid receptor in the prostate. Oncogene 2007; 26:1885-96; PMID:17016446; http://dx.doi.org/10.1038/sj.onc. 1209991.
10. Beato M, Herrlich P, Schultz G. Steroid hormone receptors: many actors in search of a plot. Cell 1995; 83:851-7; PMID:8521509; http://dx.doi.org/10.1016/ 0092-8674(95)90201-5.
11. Necela BM, Cidlowski JA. Mechanisms of glucocorticoid receptor action in non-inflammatory and inflammatory cells. Proc Am Thorac Soc 2004; 1:239-46; PMID:16113441; http://dx.doi.org/10.1513/pats.200402-005MS.
12. Tao YJ, Zheng W. Chaperones and the maturation of steroid hormone receptor complexes. Oncotarget 2011; 2:104-6; PMID:21399235.
13. Hildenbrand ZL, Molugu SK, Herrera N, Ramirez C, Xiao C, Bernal RA. Hsp90 can accommodate the simultaneous binding of the FKBP52 and HOP proteins. Oncotarget 2011; 2:43-58; PMID:21378414.
14. Adcock IM. Glucocorticoid-regulated transcription factors. Pulm Pharmacol Ther 2001; 14:211-9; PMID:11448148; http://dx.doi.org/10.1006/pupt.2001.0283.
15. De Bosscher K, Vanden BW, Haegeman G. The interplay between the glucocorticoid receptor and nuclear factorkappaB or activator protein-1: molecular mechanisms for gene repression. Endocr Rev 2003; 24:488-522; PMID:12920152; http://dx.doi.org/10.1210/er.2002-0006.
16. De Bosscher K, Vanden BW, Haegeman G. Cross-talk between nuclear receptors and nuclear factorkappaB. Oncogene 2006; 25:6868-86; PMID:17072333; http://dx.doi.org/10.1038/sj.onc.1209935.
17. Chebotaev D, Yemelyanov A, Budunova I. The mechanisms of tumor suppressor effect of glucocorticoid receptor in skin. Mol Carcinog 2007; 46:732-40; PMID:17538956; http://dx.doi.org/10.1002/mc.20349.
18. Nelius T, Filleur S, Yemeyanov A, Budunova I, Shroff E, Mirochnik Y, et al. Androgen receptor targets NFkappaB and TSP1 to suppress prostate tumor growth in vivo. Int J Cancer 2007; 121:999-1008; PMID:17487836; http://dx.doi.org/10.1002/ijc.22802.
19. Wang Q, Li W, Liu XS, Carroll JS, Jänne OA, Keeton EK, et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol Cell 2007; 27:380-92; PMID:17679089; http://dx.doi.org/10.1016/j.molcel.2007.05.041.
20. Yemelyanov A, Czwornog J, Gera L, Joshi S, Chatterton RT Jr, Budunova I. Novel steroid receptor phytomodulator compound A inhibits growth and survival of prostate cancer cells. Cancer Res 2008; 68:4763-73; PMID:18559523; http://dx.doi.org/10.1158/0008-5472.CAN-07-6104.
21. Schäcke H, Berger M, Rehwinkel H, Asadullah K. Selective glucocorticoid receptor agonists (SEGRAs): novel ligands with an improved therapeutic index. Mol Cell Endocrinol 2007; 275:109-17; PMID:17630119; http://dx.doi.org/10.1016/j.mce.2007.05.014.
22. Swart P, Swart AC, Louw A, van der Merwe KJ. Biological activities of the shrub Salsola tuberculatiformis Botsch.: contraceptive or stress alleviator? Bioessays 2003; 25:612-9; PMID:12766951; http://dx.doi.org/10.1002/bies.10285.
23. De Bosscher K, Vanden BW, Beck IM, Van MW, Hennuyer N, Hapgood J, et al. A fully dissociated compound of plant origin for inflammatory gene repression. Proc Natl Acad Sci USA 2005; 102:15827-32; PMID:16243974; http://dx.doi.org/10. 1073/pnas.0505554102.
24. Tanner TM, Verrijdt G, Rombauts W, Louw A, Hapgood JP, Claessens F. Anti-androgenic properties of Compound A, an analog of a non-steroidal plant compound. Mol Cell Endocrinol 2003; 201:155-64; PMID:12706303; http://dx.doi.org/10.1016/S0303-7207(02)00411-2.
25. Dewint P, Gossye V, De Bosscher K, Vanden Berghe W, Van Beneden K, Deforce D, et al. A plant-derived ligand favoring monomeric glucocorticoid receptor conformation with impaired transactivation potential attenuates collagen-induced arthritis. J Immunol 2008; 180:2608-15; PMID:18250472.
26. Neznanov N, Komarov AP, Neznanova L, Stanhope-Baker P, Gudkov AV. Proteotoxic stress targeted therapy (PSTT): induction of protein misfolding enhances the anti-tumor effect of the proteasome inhibitor Bortezomib. Oncotarget 2011; 2:209-21; PMID:21444945.
27. Workman P, Davies FE. A stressful life (or death): combinatorial proteotoxic approaches to cancer-selective therapeutic vulnerability. Oncotarget 2011; 2:277-80; PMID:21515932.
28. Kang Z, Pirskanen A, Ja Lnne O, Palvimo J. Involvement of Proteasome in the Dynamic Assembly of the Androgen Receptor Transcription Complex. J Biol Chem 2002; 277:48366-71; PMID:12376534; http://dx.doi.org/10.1074/jbc.M209074200.
29. Lin HK, Altuwaijri S, Lin WJ, Kan PY, Collins LL, Chang C. Proteasome activity is required for androgen receptor transcriptional activity via regulation of androgen receptor nuclear translocation and interaction with co-regulators in prostate cancer cells. J Biol Chem 2002; 277:36570-6; PMID:12119296; http://dx.doi.org/10.1074/jbc.M204751200.
30. Kinyamu HK, Jefferson WN, Archer TK. Intersection of nuclear receptors and the proteasome on the epigenetic landscape. Environ Mol Mutagen 2008; 49:83-95; PMID:18095329; http://dx.doi.org/10.1002/em.20360.
31. Wallace AD, Cidlowski JA. Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. J Biol Chem 2001; 276:42714-21; PMID:11555652; http://dx.doi.org/10.1074/jbc.M106033200.
32. Wang X, DeFranco DB. Alternative effects of the ubiquitin-proteasome pathway on glucocorticoid receptor downregulation and transactivation are mediated by CHIP, an E3 ligase. Mol Endocrinol 2005; 19:1474-82; PMID:15761032; http://dx.doi.org/10.1210/me.2004-0383.
33. Wallace AD, Cao Y, Chandramouleeswaran S, Cidlowski JA. Lysine 419 targets human glucocorticoid receptor for proteasomal degradation. Steroids 2010; 75:1016-23; PMID:20619282; http://dx.doi.org/10.1016/j.steroids.2010.06. 015.
34. Mohler JL, Chen Y, Hamil K, Hall SH, Cidlowski JA, Wilson EM, et al. Androgen and glucocorticoid receptors in the stroma and epithelium of prostatic hyperplasia and carcinoma. Clin Cancer Res 1996; 2:889-95; PMID:9816246.
35. Ikezoe T, Yang Y, Saito T, Koeffler HP, Taguchi H. Proteasome inhibitor PS-341 downregulates prostate-specific antigen (PSA) and induces growth arrest and apoptosis of androgen-dependent human prostate cancer LNCaP cells. Cancer Sci 2004; 95:271-5; PMID:15016328; http://dx.doi.org/10.1111/j.1349-7006.2004. tb02215.x.
36. Wu W, Chaudhuri S, Brickley DR, Pang D, Karrison T, Conzen SD. Microarray analysis reveals glucocorticoid-regulated survival genes that are associated with inhibition of apoptosis in breast epithelial cells. Cancer Res 2004; 64:1757-64; PMID:14996737; http://dx.doi.org/10.1158/0008-5472.CAN-03-2546.
37. UM, Shen L, Oshida T, Miyauchi J, Yamada M, Miyashita T. Identification of novel direct transcriptional targets of glucocorticoid receptor. Leukemia 2004; 18:1850-6; PMID:15385927.
38. Dong H, Chen L, Chen X, Gu H, Gao G, Gao Y, et al. Dysregulation of unfolded protein response partially underlies proapoptotic activity of Bortezomib in multiple myeloma cells. Leuk Lymphoma 2009; 50:974-84; PMID:19391038; http://dx.doi.org/10.1080/10428190902895780.
39. Davenport EL, Moore HE, Dunlop AS, Sharp SY, Workman P, Morgan GJ, et al. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 2007; 110:2641-9; PMID:17525289; http://dx.doi.org/10.1182/blood-2006-11-053728.
40. Pelley RP, Chinnakannu K, Murthy S, Strickland FM, Menon M, Dou QP, et al. Calmodulin-androgen receptor (AR) interaction: calcium-dependent, calpain-mediated breakdown of AR in LNCaP prostate cancer cells. Cancer Res 2006; 66:11754-62; PMID:17178871; http://dx.doi.org/10.1158/0008-5472.CAN-06- 2918.
41. Qi W, Wu H, Yang L, Boyd DD, Wang Z. A novel function of caspase-8 in the regulation of androgen-receptor-driven gene expression. EMBO J 2007; 26:65-75; PMID:17170703; http://dx.doi.org/10.1038/sj.emboj.7601483.
42. Yang H, Murthy S, Sarkar FH, Sheng S, Reddy GP, Dou QP. Calpain-mediated androgen receptor breakdown in apoptotic prostate cancer cells. J Cell Physiol 2008; 217:569-76; PMID:18726991; http://dx.doi.org/10.1002/jcp.21565.
43. Boccadoro M, Morgan G, Cavenagh J. Preclinical evaluation of the proteasome inhibitor bortezomib in cancer therapy. Cancer Cell Int 2005; 5:18.
44. McConkey DJ, Zhu K. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist Updat 2008; 11:164-79; PMID:18818117; http://dx.doi.org/10.1016/j.drup.2008.08.002.
45. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C, McConkey DJ. Differential effects of the proteasome inhibitor Bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther 2003; 2:835-43; PMID:14555702.
46. Schwarze SR, Lin EW, Christian PA, Gayheart DT, Kyprianou N. Intracellular death platform steps-in: targeting prostate tumors via endoplasmic reticulum (ER) apoptosis. Prostate 2008; 68:1615-23; PMID:18663729; http://dx.doi.org/10.1002/pros.20828.
47. Schäcke H, Docke WD, Asadullah K. Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 2002; 96:23-43; PMID:12441176; http://dx.doi.org/10.1016/S0163-7258(02)00297-8.
48. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998; 72:9873-80; PMID:9811723.
49. Schug J, Overton GC. Transcription Element Search Software on the WWW, Technical Report CBILTR-1997-1001-v0.0 Computational Biology and Informatics 1997; Laboratory School of Medicine University of Pennsylvania, URL: http://www.cbil.upenn.edu/tess.
50. Tanner T, Claessens F, Haelens A. The hinge region of the androgen receptor plays a role in proteasome-mediated transcriptional activation. Ann NY Acad Sci 2004; 1030:587-92; PMID:15659841; http://dx.doi.org/10.1196/annals. 1329.068.