DAX-1, as an androgen-target gene, inhibits aromatase expression: A novel mechanism blocking estrogendependent breast cancer cell proliferation

Cell Death and Disease

Volumn 4, Issue 7, 2013, Pages

  Lanzino, M ^a   Maris, P ^a   Sirianni, R ^a   Barone, I ^a   Casaburi, I ^a   Chimento, A ^a   Giordano, C ^a   Morelli, C ^a   Sisci, D ^a   Rizza, P ^a   Bonofiglio, D ^a   Catalano, S ^a   Ando, S ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

Androgen receptor; Aromatase; Breast cancer; DAX 1

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; AROMATASE; ESTROGEN; LIVER RECEPTOR HOMOLOG 1; NUCLEAR RECEPTOR COREPRESSOR; NUCLEAR RECEPTOR DAX 1; STEROIDOGENIC FACTOR 1;

ANDROGEN RESPONSE ELEMENT; ARTICLE; BREAST CANCER; CANCER CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84881055860     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.235     Document Type: Article

References (54)

1. Chen GG, Zeng Q, Tse GM. Estrogen and its receptors in cancer. Med Res Rev 2008; 28: 954-974.
2. Fowler KA, Gill K, Kirma N, Dillehay DL, Tekmal RR. Overexpression of aromatase leads to development of testicular leydig cell tumors: an in vivo model for hormone-mediated TesticularCancer. Am J Pathol 2000; 156: 347-353.
3. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006; 354: 270-282.
4. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics 2009. CA Cancer J Clin 2009; 59: 225-249.
5. Sasano H, Miki Y, Nagasaki S, Suzuki T. In situ estrogen production and its regulation in human breast carcinoma: from endocrinology to intracrinology. Pathol Int 2009; 59: 777-789.
6. Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS, Baum M. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncol 2008; 9: 45-53.
7. Park S, Koo J, Park HS, Kim JH, Choi SY, Lee JH et al. Expression of androgen receptors in primary breast cancer. Ann Oncol 2010; 21: 488-492.
8. Castellano I, Allia E, Accortanzo V, Vandone AM, Chiusa L, Arisio R et al. Androgen receptor expression is a significant prognostic factor in estrogen receptor positive breast cancers. Breast Cancer Res Treat 2010; 124: 607-617.
9. Yu Q, Niu Y, Liu N, Zhang JZ, Liu TJ, Zhang RJ et al. Expression of androgen receptor in breast cancer and its significance as a prognostic factor. Ann Oncol 2011; 22: 1288-1294.
10. Peters AA, Buchanan G, Ricciardelli C, Bianco-Miotto T, Centenera MM, Harris JM et al. Androgen receptor inhibits estrogen receptor-alpha activity and is prognostic in breast cancer. Cancer Res 2009; 69: 6131-6140.
11. Berns EM, Dirkzwager-Kiel MJ, Kuenen-Boumeester V, Timmermans M, Verhoog LC, van den Ouweland AM et al. Androgen pathway dysregulation in BRCA1-mutated breast tumors. Breast Cancer Res Treat 2003; 79: 121-127.
12. Lin Fde M, Pincerato KM, Bacchi CE, Baracat EC, Carvalho FM. Coordinated expression of oestrogen and androgen receptors in HER2-positive breast carcinomas: impact on proliferative activity. J Clin Pathol 2012; 65: 64-68.
13. Lanzino M, De Amicis F, McPhaul MJ, Marsico S, Panno ML, Ando S. Endogenous coactivator ARA70 interacts with estrogen receptor alpha (ERalpha) and modulates the functional ERalpha/androgen receptor interplay in MCF-7 cells. J Biol Chem 2005; 280: 20421-20430.
14. Ando S, De Amicis F, Rago V, Carpino A, Maggiolini M, Panno ML et al. Breast cancer: from estrogen to androgen receptor. Mol Cell Endocrinol 2002; 193: 121-128.
15. Greeve MA, Allan RK, Harvey JM, Bentel JM. Inhibition of MCF-7 breast cancer cell proliferation by 5alpha-dihydrotestosterone; a role for p21(Cip1/Waf1). J Mol Endocrinol 2004; 32: 793-810.
16. Lanzino M, Sisci D, Morelli C, Garofalo C, Catalano S, Casaburi I et al. Inhibition of cyclin D1 expression by androgen receptor in breast cancer cells-identification of a novel androgen response element. Nucleic Acids Res 2010; 38: 5351-5365.
17. Bardoni B, Zanaria E, Guioli S, Floridia G, Worley KC, Tonini G et al. A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nat Genet 1994; 7: 497-501.
18. Zanaria E, Muscatelli F, Bardoni B, Strom TM, Guioli S, GuoWet al. An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 1994; 372: 635-641.
19. Zazopoulos E, Lalli E, Stocco DM, Sassone-Corsi P. DNA binding and transcriptional repression by DAX-1 blocks steroidogenesis. Nature 1997; 390: 311-315.
20. Guo W, Burris TP, McCabe ER. Expression of DAX-1, the gene responsible for X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism, in the hypothalamicpituitary-adrenal/gonadal axis. Biochem Mol Med 1995; 56: 8-13.
21. Lalli E, Sassone-Corsi P. DAX-1, an unusual orphan receptor at the crossroads of steroidogenic function and sexual differentiation. Mol Endocrinol 2003; 17: 1445-1453.
22. Crawford PA, Dorn C, Sadovsky Y, Milbrandt J. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 1998; 18: 2949-2956.
23. Hanley NA, Rainey WE, Wilson DI, Ball SG, Parker KL. Expression profiles of SF-1, DAX1, and CYP17 in the human fetal adrenal gland: potential interactions in gene regulation. Mol Endocrinol 2001; 15: 57-68.
24. Wang ZJ, Jeffs B, Ito M, Achermann JC, Yu RN, Hales DB et al. Aromatase (Cyp19) expression is up-regulated by targeted disruption of Dax1. Proc Natl Acad Sci USA 2001; 98: 7988-7993.
25. Reincke M, Beuschlein F, Lalli E, Arlt W, Vay S, Sassone-Corsi P et al. DAX-1 expression in human adrenocortical neoplasms: implications for steroidogenesis. J Clin Endocrinol Metab 1998; 83: 2597-2600.
26. Chae BJ, Lee A, Bae JS, Song BJ, Jung SS. Expression of nuclear receptor DAX-1 and androgen receptor in human breast cancer. J Surg Oncol 2011; 103: 768-772.
27. Conde I, Alfaro JM, Fraile B, Ruiz A, Paniagua R, Arenas MI. DAX-1 expression in human breast cancer: comparison with estrogen receptors ER-alpha, ER-beta and androgen receptor status. Breast Cancer Res 2004; 6: R140-R148.
28. Park YY, Ahn SW, Kim HJ, Kim JM, Lee IK, Kang H et al. An autoregulatory loop controlling orphan nuclear receptor DAX-1 gene expression by orphan nuclear receptor ERRgamma. Nucleic Acids Res 2005; 33: 6756-6768.
29. Abd-Elaziz M, Akahira J, Moriya T, Suzuki T, Yaegashi N, Sasano H. Nuclear receptor DAX-1 in human common epithelial ovarian carcinoma: an independent prognostic factor of clinical outcome. Cancer Sci 2003; 94: 980-985.
30. Saito S, Ito K, Suzuki T, Utsunomiya H, Akahira J, Sugihashi Y et al. Orphan nuclear receptor DAX-1 in human endometrium and its disorders. Cancer Sci 2005; 96: 645-652.
31. Nakamura Y, Suzuki T, Arai Y, Sasano H. Nuclear receptor DAX1 in human prostate cancer: a novel independent biological modulator. Endocr J 2009; 56: 39-44.
32. Zoppi S, Marcelli M, Deslypere JP, Griffin JE, Wilson JD, McPhaul MJ. Amino acid substitutions in the DNA-binding domain of the human androgen receptor are a frequent cause of receptor-binding positive androgen resistance. Mol Endocrinol 1992; 6: 409-415.
33. Verrijdt G, Haelens A, Claessens F. Selective DNA recognition by the androgen receptor as a mechanism for hormone-specific regulation of gene expression. Mol Genet Metab 2003; 78: 175-185.
34. Sirianni R, Chimento A, Malivindi R, Mazzitelli I, Ando S, Pezzi V. Insulin-like growth factor-I, regulating aromatase expression through steroidogenic factor 1, supports estrogendependent tumor Leydig cell proliferation. Cancer Res 2007; 67: 8368-8377.
35. Sasano H, Harada N. Intratumoral aromatase in human breast, endometrial, and ovarian malignancies. Endocr Rev 1998; 19: 593-607.
36. Barone I, Giordano C, Malivindi R, Lanzino M, Rizza P, Casaburi I et al. Estrogens and PTP1B function in a novel pathway to regulate aromatase enzymatic activity in breast cancer cells. Endocrinology 2012; 153: 5157-5166.
37. Clipsham R, McCabe ER. DAX1 and its network partners: exploring complexity in development. Mol Genet Metab 2003; 80: 81-120.
38. Ikeda Y, Swain A, Weber TJ, Hentges KE, Zanaria E, Lalli E et al. Steroidogenic factor 1 and Dax-1 colocalize in multiple cell lineages: potential links in endocrine development. Mol Endocrinol 1996; 10: 1261-1272.
39. Lalli E, Melner MH, Stocco DM, Sassone-Corsi P. DAX-1 blocks steroid production at multiple levels. Endocrinology 1998; 139: 4237-4243.
40. Zhang H, Slewa A, Janssen E, Skaland I, Yu Y, Gudlaugsson E et al. The prognostic value of the orphan nuclear receptor DAX-1 (NROB1) in node-negative breast cancer. Anticancer Res 2011; 31: 443-449.
41. Tamai KT, Monaco L, Alastalo TP, Lalli E, Parvinen M, Sassone-Corsi P. Hormonal and developmental regulation of DAX-1 expression in Sertoli cells. Mol Endocrinol 1996; 10: 1561-1569.
42. Suzuki T, Miki Y, Moriya T, Akahira J, Ishida T, Hirakawa H et al. 5Alpha-reductase type 1 and aromatase in breast carcinoma as regulators of in situ androgen production. Int J Cancer 2007; 120: 285-291.
43. Takagi K, Miki Y, Nagasaki S, Hirakawa H, Onodera Y, Akahira J et al. Increased intratumoral androgens in human breast carcinoma following aromatase inhibitor exemestane treatment. Endocr Relat Cancer 2010; 17: 415-430.
44. Rovito D, Giordano C, Vizza D, Plastina P, Barone I, Casaburi I et al. Omega-3 PUFA ethanolamides DHEA and EPEA induce autophagy through PPARg activation in MCF-7 breast cancer cells. J Cell Physiol 2013; 228: 1314-1322.
45. Catalano S, Panza S, Malivindi R, Giordano C, Barone I, Bossi G et al. Inhibition of Leydig tumor growth by farnesoid X receptor activation: the in vitro and in vivo basis for a novel therapeutic strategy. Int J Cancer 2013; 132: 2237-2247.
46. Recchia AG, Musti AM, Lanzino M, Panno ML, Turano E, Zumpano R et al. A cross-talk between the androgen receptor and the epidermal growth factor receptor leads to p38 MAPK-dependent activation of mTOR and cyclinD1 expression in prostate and lung cancer cells. Int J Biochem Cell Biol 2009; 41: 603-614.
47. Guido C, Panza S, Santoro M, Avena P, Panno ML, Perrotta I et al. Estrogen receptor beta (ERb) produces autophagy and necroptosis in human seminoma cell line through the binding of the Sp1 on the phosphatase and tensin homolog deleted from chromosome 10 (PTEN) promoter gene. Cell Cycle 2012; 11: 2911-2921.
48. Lanzino M, Garofalo C, Morelli C, Le Pera M, Casaburi I, McPhaul MJ et al. Insulin receptor substrate 1 modulates the transcriptional activity and the stability of androgen receptor in breast cancer cells. Breast Cancer Res Treat 2009; 115: 297-306.
49. Chimento A, Sirianni R, Zolea F, De Luca A, Lanzino M, Catalano S et al. Nandrolone and stanozolol induce Leydig cell tumor proliferation through an estrogen-dependent mechanism involving IGF-I system. J Cell Physiol 2012; 227: 2079-2088.
50. Barone I, Catalano S, Gelsomino L, Marsico S, Giordano C, Panza S et al. Leptin mediates tumor-stromal interactions that promote the invasive growth of breast cancer cells. Cancer Res 2012; 72: 1416-1427.
51. Morelli C, Lanzino M, Garofalo C, Maris P, Brunelli E, Casaburi I et al. Akt2 inhibition enables the forkhead transcription factor FoxO3a to have a repressive role in estrogen receptor alpha transcriptional activity in breast cancer cells. Mol Cell Biol 2010; 30: 857-870.
52. Giordano C, Vizza D, Panza S, Barone I, Bonofiglio D, Lanzino M et al. Leptin increases HER2 protein levels through a STAT3-mediated up-regulation of Hsp90 in breast cancer cells. Mol Oncol 2012; pii: S1574-7891: 00123-00128.
53. Catalano S, Rizza P, Gu G, Barone I, Giordano C, Marsico S et al. Fas ligand expression in TM4 Sertoli cells is enhanced by estradiol 'in situ' production. J Cell Physiol 2007; 211: 448-456.
54. Casaburi I, Avena P, Lanzino M, Sisci D, Giordano F, Maris P et al. Chenodeoxycholic acid through a TGR5-dependent CREB signaling activation enhances cyclin D1 expression and promotes human endometrial cancer cell proliferation. Cell Cycle 2012; 11: 2699-2710.