Insulin receptor substrate 1 modulates the transcriptional activity and the stability of androgen receptor in breast cancer cells

Breast Cancer Research and Treatment

Volumn 115, Issue 2, 2009, Pages 297-306

  Lanzino, Marilena ^a   Garofalo, Cecilia ^a   Morelli, Catia ^a   Le Pera, Maria ^b   Casaburi, Ivan ^a   McPhaul, Michael J ^c   Surmacz, Eva ^d   Andò, Sebastiano ^a   Sisci, Diego ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b INSTITUTE OF NEUROLOGICAL SCIENCES   (Italy)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d TEMPLE UNIVERSITY   (United States)

Author keywords

Androgen receptor; Breast cancer; IGF I; IRS 1

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANOLONE; INSULIN RECEPTOR SUBSTRATE 1; PROTEASOME; UBIQUITIN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CELL NUCLEUS TRANSPLANTATION; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; EMBRYO; GENETIC TRANSCRIPTION; HORMONAL REGULATION; HORMONE ACTION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN STABILITY;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DIHYDROTESTOSTERONE; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPRECIPITATION; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICROSCOPY, CONFOCAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION, GENETIC;

EID: 67349178258     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-008-0079-1     Document Type: Article

References (51)

1. SM Aronica BS Katzenellenbogen 1993 Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I Mol Endocrinol 7 743 752 10.1210/me.7.6.743
2. DM Ignar-Trowbridge CT Teng KA Ross 1993 Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element Mol Endocrinol 7 992 998 10.1210/me.7.8.992
3. KB Reddy D Yee SG Hilsenbeck 1994 Inhibition of estrogen-induced breast cancer cell proliferation by reduction in autocrine transforming growth factor alpha expression Cell Growth Differ 5 1275 1282
4. JK Ruohola EM Valve MJ Karkkainen 1999 Vascular endothelial growth factors are differentially regulated by steroid hormones and antiestrogens in breast cancer cells Mol Cell Endocrinol 149 29 40 10.1016/S0303-7207(99)00003-9
5. D Sisci E Surmacz 2007 Crosstalk between IGF signaling and steroid hormone receptors in breast cancer Curr Pharm Des 13 705 717 10.2174/138161207780249182
6. SN Birrell JM Bentel TE Hickey 1995 Androgens induce divergent proliferative responses in human breast cancer cell lines J Steroid Biochem Mol Biol 52 459 467 10.1016/0960-0760(95)00005-K
7. F Labrie V Luu-The C Labrie 2003 Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone Endocr Rev 24 152 182 10.1210/er.2001-0031
8. C Dimitrakakis J Zhou J Wang 2003 A physiologic role for testosterone in limiting estrogenic stimulation of the breast Menopause 10 292 298 10.1097/01.GME.0000055522.67459.89
9. LC Murphy P Watson 2002 Steroid receptors in human breast tumorigenesis and breast cancer progression Biomed Pharmacother 56 65 77 10.1016/S0753- 3322(01)00157-3
10. S Ando F De Amicis V Rago 2002 Breast cancer: from estrogen to androgen receptor Mol Cell Endocrinol 193 121 128 10.1016/S0303-7207(02)00105-3
11. J Ortmann S Prifti MK Bohlmann 2002 Testosterone and 5-alpha- dihydrotestosterone inhibit in vitro growth of human breast cancer cell lines Gynecol Endocrinol 16 113 120 10.1080/713603030
12. M Lanzino F De Amicis MJ McPhaul 2005 Endogenous coactivator ARA70 interacts with estrogen receptor alpha (ERalpha) and modulates the functional ERalpha/androgen receptor interplay in MCF-7 cells J Biol Chem 280 20421 20430 10.1074/jbc.M413576200
13. V Kuenen-Boumeester TH Van der Kwast WL van Putten 1992 Immunohistochemical determination of androgen receptors in relation to oestrogen and progesterone receptors in female breast cancer Int J Cancer 52 581 584 10.1002/ijc.2910520415
14. OA Lea S Kvinnsland T Thorsen 1989 Improved measurement of androgen receptors in human breast cancer Cancer Res 49 7162 7167
15. CM Wilson MJ McPhaul 1996 A and B forms of the androgen receptor are expressed in a variety of human tissues Mol Cell Endocrinol 120 51 57 10.1016/0303-7207(96)03819-1
16. IB Bayer-Garner B Smoller 2000 Androgen receptors: a marker to increase sensitivity for identifying breast cancer in skin metastasis of unknown primary site Mod Pathol 13 119 122 10.1038/modpathol.3880021
17. RM Bryan RJ Mercer RC Bennett 1984 Androgen receptors in breast cancer Cancer 54 2436 2440 10.1002/1097-0142(19841201)54:11 ≤ 2436::AID- CNCR2820541121 ≥ 3.0.CO;2-H
18. EM Berns MJ Dirkzwager-Kiel V Kuenen-Boumeester 2003 Androgen pathway dysregulation in BRCA1-mutated breast tumors Breast Cancer Res Treat 79 121 127 10.1023/A:1023347409599
19. A Kollara HJ Kahn A Marks 2001 Loss of androgen receptor associated protein 70 (ARA70) expression in a subset of HER2-positive breast cancers Breast Cancer Res Treat 67 245 253 10.1023/A:1017938608460
20. C Morelli C Garofalo D Sisci 2004 Nuclear insulin receptor substrate 1 interacts with estrogen receptor alpha at ERE promoters Oncogene 23 7517 7526 10.1038/sj.onc.1208014
21. E Surmacz 2000 Function of the IGF-I receptor in breast cancer J Mammary Gland Biol Neoplasia 5 95 105 10.1023/A:1009523501499
22. D Sachdev D Yee 2001 The IGF system and breast cancer Endocr Relat Cancer 8 197 209 10.1677/erc.0.0080197
23. A Lassak L Del Valle F Peruzzi 2002 Insulin receptor substrate 1 translocation to the nucleus by the human JC virus T-antigen J Biol Chem 277 17231 17238 10.1074/jbc.M110885200
24. D Sisci C Morelli C Garofalo 2006 Expression of nuclear insulin receptor substrate 1 (IRS-1) in breast cancer J Clin Pathol 60 633 641
25. H Sun X Tu M Prisco 2003 Insulin-like growth factor I receptor signaling and nuclear translocation of insulin receptor substrates 1 and 2 Mol Endocrinol 17 472 486 10.1210/me.2002-0276
26. X Tu P Batta N Innocent 2002 Nuclear translocation of insulin receptor substrate-1 by oncogenes and Igf-I. Effect on ribosomal RNA synthesis. J Biol Chem 277 44357 44365 10.1074/jbc.M208001200
27. WD Tilley M Marcelli MJ McPhaul 1990 Expression of the human androgen receptor gene utilizes a common promoter in diverse human tissues and cell lines J Biol Chem 265 13776 13781
28. G Cesarone C Garofalo MT Abrams 2006 RNAi-mediated silencing of insulin receptor substrate 1 (IRS-1) enhances tamoxifen-induced cell death in MCF-7 breast cancer cells J Cell Biochem 98 440 450 10.1002/jcb.20817
29. C Laban SA Bustin PJ Jenkins 2003 The GH-IGF-I axis and breast cancer Trends Endocrinol Metab 14 28 34 10.1016/S1043-2760(02)00003-6
30. MA Greeve RK Allan JM Harvey 2004 Inhibition of MCF-7 breast cancer cell proliferation by 5alpha-dihydrotestosterone; a role for p21(Cip1/Waf1) J Mol Endocrinol 32 793 810 10.1677/jme.0.0320793
31. KB Cleutjens CC van Eekelen HA van der Korput 1996 Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter J Biol Chem 271 6379 6388 10.1074/jbc.271.11.6379
32. MH Black EP Diamandis 2000 The diagnostic and prognostic utility of prostate-specific antigen for diseases of the breast Breast Cancer Res Treat 59 1 14 10.1023/A:1006380306781
33. S Lu M Liu DE Epner 1999 Androgen regulation of the cyclin-dependent kinase inhibitor p21 gene through an androgen response element in the proximal promoter Mol Endocrinol 13 376 384 10.1210/me.13.3.376
34. KK Takane MJ McPhaul 1996 Functional analysis of the human androgen receptor promoter Mol Cell Endocrinol 119 83 93 10.1016/0303-7207(96)03800-2
35. JL Dai KL Burnstein 1996 Two androgen response elements in the androgen receptor coding region are required for cell-specific up-regulation of receptor messenger RNA Mol Endocrinol 10 1582 1594 10.1210/me.10.12.1582
36. RN Freiman R Tjian 2003 Regulating the regulators: lysine modifications make their mark Cell 112 11 17 10.1016/S0092-8674(02)01278-3
37. Z Nawaz BW O'Malley 2004 Urban renewal in the nucleus: is protein turnover by proteasomes absolutely required for nuclear receptor-regulated transcription? Mol Endocrinol 18 493 499 10.1210/me.2003-0388
38. AV Lee JL Gooch S Oesterreich 2000 Insulin-like growth factor I-induced degradation of insulin receptor substrate 1 is mediated by the 26S proteasome and blocked by phosphatidylinositol 3?-kinase inhibition Mol Cell Biol 20 1489 1496 10.1128/MCB.20.5.1489-1496.2000
39. H Zhang H Hoff C Sell 2000 Insulin-like growth factor I-mediated degradation of insulin receptor substrate-1 is inhibited by epidermal growth factor in prostate epithelial cells J Biol Chem 275 22558 22562 10.1074/jbc.M000412200
40. S Burgdorf P Leister KH Scheidtmann 2004 TSG101 interacts with apoptosis-antagonizing transcription factor and enhances androgen receptor-mediated transcription by promoting its monoubiquitination J Biol Chem 279 17524 17534 10.1074/jbc.M313703200
41. L Gaughan IR Logan DE Neal 2005 Regulation of androgen receptor and histone deacetylase 1 by Mdm2-mediated ubiquitylation Nucleic Acids Res 33 13 26 10.1093/nar/gki141
42. HK Lin L Wang YC Hu 2002 Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase EMBO J 21 4037 4048 10.1093/emboj/cdf406
43. VJ Palombella OJ Rando AL Goldberg 1994 The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B Cell 78 773 785 10.1016/S0092-8674(94)90482-0
44. E Surmacz JL Burgaud 1995 Overexpression of insulin receptor substrate 1 (IRS-1) in the human breast cancer cell line MCF-7 induces loss of estrogen requirements for growth and transformation Clin Cancer Res 1 1429 1436
45. Schnarr B, Strunz K, Ohsam J, et al (2000) Down-regulation of insulin-like growth factor-I receptor and insulin receptor substrate-1 expression in advanced human breast cancer. Int J Cancer 89:506-513. doi :10.1002/1097-0215(20001120)89:6≤506::AID-IJC7≥3.0.CO;2-F
46. OW Prall B Sarcevic EA Musgrove 1997 Estrogen-induced activation of Cdk4 and Cdk2 during G1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibitor association with cyclin E-Cdk2 J Biol Chem 272 10882 10894 10.1074/jbc.272.16.10882
47. AJ Skildum S Mukherjee SE Conrad 2002 The cyclin-dependent kinase inhibitor p21WAF1/Cip1 is an antiestrogen-regulated inhibitor of Cdk4 in human breast cancer cells J Biol Chem 277 5145 5152 10.1074/jbc.M109179200
48. RL Rocha SG Hilsenbeck JG Jackson 1997 Insulin-like growth factor binding protein-3 and insulin receptor substrate-1 in breast cancer: correlation with clinical parameters and disease-free survival Clin Cancer Res 3 103 109
49. J Trojanek T Ho S Croul 2006 IRS-1-Rad51 nuclear interaction sensitizes JCV T-antigen positive medulloblastoma cells to genotoxic treatment Int J Cancer 119 539 548 10.1002/ijc.21828
50. F Pajonk A van Ophoven C Weissenberger 2005 The proteasome inhibitor MG-132 sensitizes PC-3 prostate cancer cells to ionizing radiation by a DNA-PK-independent mechanism BMC Cancer 5 76 10.1186/1471-2407-5-76
51. GP Reddy ER Barrack QP Dou 2006 Regulatory processes affecting androgen receptor expression, stability, and function: Potential targets to treat hormone-refractory prostate cancer J Cell Biochem 98 1408 1423