Steroidogenic factor 1 promotes aggressive growth of castration-resistant prostate cancer cells by stimulating steroid synthesis and cell proliferation

Endocrinology

Volumn 155, Issue 2, 2014, Pages 358-369

  Lewis, Samantha R ^a   Hedman, Curtis J ^c,d,e   Ziegler, Toni ^d,e   Ricke, William A ^b,e   Jorgensen, Joan S ^a,b,e  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c WISCONSIN STATE LABORATORY OF HYGIENE   (United States)

^d UNIVERSITY OF WISCONSIN   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABIRATERONE; SHORT HAIRPIN RNA; STEROID; STEROIDOGENIC FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CASTRATION RESISTANT PROSTATE CANCER; CELL PROLIFERATION; CELL STIMULATION; CENTROSOME; CONTROLLED STUDY; GENE SILENCING; HOMEOSTASIS; HOST; HUMAN; HUMAN CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROSTATE EPITHELIUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; STEROIDOGENESIS; TUMOR XENOGRAFT;

ANDROGENS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; PROSTATE; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; STEROIDOGENIC FACTOR 1;

EID: 84893197963     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1583     Document Type: Article

References (86)

1. Huggins C, Hodges CV. Studies on prostatic cancer. I. The effect of castration, of estrogenandofandrogeninjectiononserumphosphatasesin metastatic carcinoma of the prostate. Cancer Res. 1941;1: 293-297.
2. Tammela T. Endocrine treatment of prostate cancer. J Steroid Biochem Mol Biol. 2004;92: 287-295.
3. Attard G, Cooper CS, de Bono JS. Steroid hormone receptors in prostate cancer: a hard habit to break? Cancer Cell. 2009;16: 458-462.
4. Visakorpi T, Hyytinen E, Koivisto P, et al. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet. 1995;9: 401-406.
5. Ueda T, Mawji NR, Bruchovsky N, SadarMD.Ligand-independent activation of the androgen receptor by interleukin-6 and the role of steroid receptor coactivator-1 in prostate cancer cells. J Biol Chem. 2002;277: 38087-38094.
6. Debes JD, Tindall DJ. Mechanisms of androgen-refractory prostate cancer. N Engl J Med. 2004;351: 1488-1490.
7. Zhang X, Morrissey C, Sun S, et al. Androgen receptor variants occur frequently in castration resistant prostate cancer metastases. PLoSOne. 2011;6:e27970.
8. Steinkamp MP, O'Mahony OA, Brogley M, et al. Treatment-dependent androgen receptor mutations in prostate cancer exploit multiple mechanisms to evade therapy. Cancer Res. 2009;69: 4434-4442.
9. Vis AN, Schröder FH. Key targets of hormonal treatment of prostate cancer. Part 1: the androgen receptor and steroidogenic pathways. BJU Int. 2009;104: 438-448.
10. Montgomery RB, Mostaghel EA, Vessella R, et al. Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth. Cancer Res. 2008;68: 4447-4454.
11. Stanbrough M, Bubley GJ, Ross K, et al. Increased expression of genes converting adrenal androgens to testosterone in androgenindependent prostate cancer. Cancer Res. 2006;66: 2815-2825.
12. Locke JA, Guns ES, Lubik AA, et al. Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration- resistant prostate cancer. Cancer Res. 2008;68: 6407-6415.
13. Hoivik EA, Lewis AE, Aumo L, Bakke M. Molecular aspects of steroidogenic factor 1 (SF-1). Mol Cell Endocrinol. 2010;315: 27-39.
14. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell. 1994;77: 481-490.
15. Ikeda Y, Lala DS, Luo X, Kim E, Moisan MP, Parker KL. Characterization of the mouse FTZ-F1 gene, which encodes a key regulator of steroid hydroxylase gene expression. Mol Endocrinol. 1993;7: 852-860.
16. Morohashi K, Iida H, Nomura M, et al. Functional difference between Ad4BP and ELP, and their distributions in steroidogenic tissues. Mol Endocrinol. 1994;8: 643-653.
17. Lala DS, Rice DA, Parker KL. Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol Endocrinol. 1992;6: 1249-1258.
18. Morohashi K, Honda S, Inomata Y, Handa H,OmuraT.Acommon trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem. 1992;267: 17913-17919.
19. Honda S, Morohashi K, NomuraM,Takeya H, KitajimaM,Omura T.Ad4BPregulating steroidogenic P-450 gene is amemberof steroid hormone receptor superfamily. J Biol Chem 1993;268: 7494-7502.
20. Bakke M, Lund J. Mutually exclusive interactions of two nuclear orphan receptors determine activity of a cyclic adenosine 3',5'- monophosphate- responsive sequence in the bovine CYP17 gene. Mol Endocrinol. 1995;9: 327-339.
21. Mascaró C, Nadal A, Hegardt FG, Marrero PF, Haro D. Contribution of steroidogenic factor 1 to the regulation of cholesterol synthesis. Biochem. J. 2000;350(Pt 3): 785-790.
22. Schimmer BP, White PC. Minireview: Steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol. 2010;24: 1322-1337.
23. O'Shaughnessy PJ, Baker P, Sohnius U, Haavisto AM, Charlton HM, Huhtaniemi I. Fetal development of Leydig cell activity in the mouse is independent of pituitary gonadotroph function. Endocrinology. 1998;139: 1141-1146.
24. Ferraz-de-Souza B, Lin L, Achermann JC. Steroidogenic factor-1 (SF-1, NR5A1) and human disease. Mol Cell Endocrinol. 2011; 336: 198-205.
25. Laufer E, Kesper D, Vortkamp A, King P. Sonic hedgehog signaling during adrenal development. Mol Cell Endocrinol. 2012;351: 19-27.
26. Huang CCJ, Yao HH. Diverse functions of Hedgehog signaling in formation and physiology of steroidogenic organs. Mol Reprod Dev. 2010;77: 489-496.
27. Buaas FW, Gardiner JR, Clayton S, Val P, Swain A. In vivo evidence for the crucial role of SF1 in steroid-producing cells of the testis, ovary and adrenal gland. Development. 2012;139: 4561-4570.
28. Jeyasuria P, Ikeda Y, Jamin SP, et al. Cell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol. 2004;18: 1610-1619.
29. Zhao L, Bakke M, Hanley NA, et al. Tissue-specific knockouts of steroidogenic factor 1. Mol Cell Endocrinol. 2004;215: 89-94.
30. Mello MP, França ES, Fabbri HC, Maciel-Guerra AT, Guerra-Júnior G. Multifunctional role of steroidogenic factor 1 and disorders of sex development. Arq Bras Endocrinol Metabol. 2011;55: 607-612.
31. Ozisik G, Achermann JC, Jameson JL. The role of SF1 in adrenal and reproductive function: insight from naturally occurring mutations in humans. Mol Genet Metab. 2002;76: 85-91.
32. Achermann JC, Ito M, Ito M, Hindmarsh PC, Jameson JL.Amutation in the gene encoding steroidogenic factor-1 causesXYsex reversal and adrenal failure in humans. Nat Genet. 1999;22: 125-126.
33. Crawford PA, Sadovsky Y, Milbrandt J. Nuclear receptor steroidogenic factor 1 directs embryonic stem cells toward the steroidogenic lineage. Mol Cell Biol. 1997;17: 3997-4006.
34. Yazawa T, Mizutani T, Yamada K, et al. Differentiation of adult stem cells derived from bone marrow stroma into Leydig or adrenocortical cells. Endocrinology. 2006;147: 4104-4111.
35. GondoS,OkabeT, Tanaka T, et al. Adipose tissue-derived and bone marrow-derived mesenchymal cells develop into different lineage of steroidogenic cells by forced expression of steroidogenic factor 1. Endocrinology. 2008;149: 4717-4725.
36. Doghman M, Karpova T, Rodrigues GA, et al. Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol. 2007;21: 2968-2987.
37. Ramayya MS, Sheng M, Moroz K, Hill SM, Rowan BG. Human steroidogenic factor-1 (hSF-1) regulates progesterone biosynthesis and growth of ovarian surface epithelial cancer cells. J Steroid Biochem Mol Biol. 2010;119: 14-25.
38. Zeitoun K, Takayama K, Michael MD, Bulun SE. Stimulation of aromatase P450 promoter (II) activity in endometriosis and its inhibition in endometrium are regulated by competitive binding of steroidogenic factor-1 and chicken ovalbumin upstream promoter transcription factor to the same cis-acting element. MolEndocrinol. 1999;13: 239-253.
39. Ikeda Y, Shen WH, Ingraham HA, Parker KL. Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol. 1994;8: 654-662.
40. Ikeda Y, Luo X, Abbud R, Nilson JH, Parker KL. The nuclear receptor steroidogenic factor 1 is essential for the formation of the ventromedial hypothalamic nucleus. Mol Endocrinol. 1995;9: 478-486.
41. Sadovsky Y, Crawford PA, Woodson KG, et al. Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 side-chain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc Natl Acad Sci USA. 1995;92: 10939-10943.
42. Ingraham HA, Lala DS, Ikeda Y, et al. The nuclear receptor steroidogenic factor 1 acts at multiple levels of the reproductive axis. Genes Dev. 1994;8: 2302-2312.
43. Wang CY, Chen WY, Lai PY, Chung BC. Distinct functions of steroidogenic factor-1 (NR5A1) in the nucleus and the centrosome. Mol Cell Endocrinol. 2013;371: 148-153.
44. Lai PY, Wang CY, Chen WY, et al. Steroidogenic factor 1 (NR5A1) resides in centrosomes and maintains genomic stability by controlling centrosome homeostasis. Cell Death Differ. 2011;18: 1836-1844.
45. KimJH, Lee SR, Li LH, et al. High cleavage efficiency of a 2Apeptide derived from porcine teschovirus-1 inhumancell lines, zebrafish and mice. PLoS One. 2011;6:e18556.
46. Jorgensen JS, Nilson JH. AR suppresses transcription of the LHβ subunit by interacting with steroidogenic factor-1. Mol Endocrinol. 2001;15: 1505-1516.
47. Hayward SW, Dahiya R, Cunha GR, Bartek J, Deshpande N, Narayan P. Establishment and characterization of an immortalized but non-transformed human prostate epithelial cell line: BPH-1. In Vitro Cell Dev Biol Anim. 1995;31: 14-24.
48. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods. 2001;25: 402-408.
49. Wang Y, Sudilovsky D, Zhang B, et al. A human prostatic epithelial model of hormonal carcinogenesis. Cancer Res. 2001;61: 6064-6072.
50. Ricke WA, Ishii K, Ricke EA, et al. Steroid hormones stimulate human prostate cancer progression and metastasis. Int J Cancer. 2006;118: 2123-2131.
51. Franco OE, Jiang M, Strand DW, et al. Altered TGF-β signaling in a subpopulation of human stromal cells promotes prostatic carcinogenesis. Cancer Res. 2011;71: 1272-1281.
52. Stone KR, Mickey DD, Wunderli H, Mickey GH, Paulson DF. Isolation of a human prostate carcinoma cell line (DU 145). Int J Cancer. 1978;21: 274-281.
53. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 1979;17: 16-23.
54. Horoszewicz JS, Leong SS, Chu TM, et al. The LNCaP cell line-a new model for studies onhumanprostatic carcinoma. Prog Clin Biol Res. 1980;37: 115-132.
55. Torres JM, Ortega E. Differential regulation of steroid 5α-reductase isozymes expression by androgens in the adult rat brain. FASEB J. 2003;17: 1428-1433.
56. Young M, McPhaul MJ. A steroidogenic factor-1-binding site and cyclic adenosine 3',5'-monophosphate response element-like elements are required for the activity of the rat aromatase promoter in rat Leydig tumor cell lines. Endocrinology. 1998;139: 5082-5093.
57. Doghman M, Cazareth J, Douguet D, Madoux F, Hodder P, Lalli E. Inhibition of adrenocortical carcinoma cell proliferation by steroidogenic factor-1 inverse agonists. J Clin Endocrinol Metab. 2009; 94: 2178-2183.
58. Barrie SE, Potter GA, Goddard PM, Haynes BP, DowsettM,Jarman M. Pharmacology of novel steroidal inhibitors of cytochrome P45017α (17α-hydroxylase/C17-20 lyase). J Steroid Biochem Mol Biol. 1994;50: 267-273.
59. Potter GA, Barrie SE, Jarman M, Rowlands MG. Novel steroidal inhibitors of human cytochrome P45017α (17α-hydroxylase- C17,20-lyase): potential agents for the treatment of prostatic cancer. J Med Chem. 1995;38: 2463-2471.
60. Rowlands MG, Barrie SE, Chan F, et al. Esters of 3-pyridylacetic acid that combine potent inhibition of 17α-hydroxylase/C17,20- lyase (cytochrome P45017α) with resistance to esterase hydrolysis. J Med Chem. 1995;38: 4191-4197.
61. Busygina TV, Vasiliev GV, Klimova NV, Ignatieva EV, Osadchuk AV. Binding sites for transcription factor SF-1 in promoter regions of genes encoding mouse steroidogenesis enzymes 3βHSDI and P450c17. Biochemistry Mosc. 2005;70: 1152-1156.
62. Li LA, Chang YC, Wang CJ, Tsai FY, Jong SB, Chung BC. Steroidogenic factor 1 differentially regulates basal and inducible steroidogenic gene expression and steroid synthesis in human adrenocortical H295R cells. J Steroid Biochem Mol Biol. 2004;91: 11-20.
63. Ito M., Richard NY, Jameson JL. Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol Endocrinol. 1998;12: 290-301.
64. Ito M, Park Y, Weck J, Mayo KE, Jameson JL. Synergistic activation of the inhibinα-promoter by steroidogenic factor-1 and cyclic adenosine 3',5'-monophosphate. Mol Endocrinol. 2000;14: 66-81.
65. HammerGD,Krylova I,ZhangY, et al. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol Cell. 1999;3: 521-526.
66. Jacob AL, Lund J, Martinez P, Hedin L. Acetylation of steroidogenic factor 1 protein regulates its transcriptional activity and recruits the coactivator GCN5. J Biol Chem. 2001;276: 37659-37664.
67. Chen WY, Juan LJ, Chung BC. SF-1 (nuclear receptor 5A1) activity is activated by cyclic AMP via p300-mediated recruitment to active foci, acetylation, and increased DNA binding. Mol Cell Biol. 2005; 25: 10442-10453.
68. Sakai N, Terami H, Suzuki S, et al. Identification of NR5A1 (SF-1/ AD4BP) gene expression modulators by large-scale gain and loss of function studies. J Endocrinol. 2008;198: 489-497.
69. de Bono JS, Logothetis CJ, Molina A, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med. 2011; 364: 1995-2005.
70. Attard G, Reid AH, A'Hern R, et al. Selective inhibition of CYP17 with abiraterone acetate is highly active in the treatment of castration- resistant prostate cancer. J Clin Oncol. 2009;27: 3742-3748.
71. Attard G, Belldegrun AS, de Bono JS. Selective blockade of androgenic steroid synthesis by novel lyase inhibitors as a therapeutic strategy for treating metastatic prostate cancer. BJU Int. 2005;96: 1241-1246.
72. Mostaghel, EA, Marck BT, Plymate SR, et al. Resistance to CYP17A1 inhibition with abiraterone in castration-resistant prostate cancer: induction of steroidogenesis and androgen receptor splice variants. Clin Cancer Res. 2011;17: 5913-5925.
73. Cai C, Chen S, Ng P, et al. Intratumoral de novo steroid synthesis activates androgen receptor in castration-resistant prostate cancer and is upregulated by treatment with CYP17A1 inhibitors. Cancer Res. 2011;71: 6503-6513.
74. Wilding G. 1995. Endocrine control of prostate cancer. Cancer Surv. 1995;23:43-62
75. MongeA, JaglaM,Lapouge G, et al. Unfaithfulness and promiscuity of a mutant androgen receptor in a hormone-refractory prostate cancer. Cell Mol Life Sci. 2006;63: 487-497.
76. Southwell J, Chowdhury SF, Gottlieb B, et al. An investigation into CAG repeat length variation and N/C terminal interactions in the T877Amutant androgen receptor found in prostate cancer. J Steroid Biochem Mol Biol. 2008;111: 138-146.
77. Ellem SJ, Risbridger GP. Treating prostate cancer: a rationale for targeting local oestrogens. Nat Rev Cancer. 2007;7: 621-627.
78. Vu Hai MT, Warembourg M, Milgrom E. Hormonal control of progesterone receptors. Ann NY Acad Sci. 1977;286: 199-209.
79. Wang CY, Kao YH, Lai PY, Chen WY, Chung BC. Steroidogenic factor 1 (NR5A1) maintains centrosome homeostasis in steroidogenic cells by restricting centrosomal DNA-dependent protein kinase activation. Mol Cell Biol. 2013;33: 476-484.
80. Del Tredici AL, Andersen CB, Currier EA, et al. Identification of the first synthetic steroidogenic factor 1 inverse agonists: pharmacological modulation of steroidogenic enzymes. Mol Pharmacol. 2008; 73: 900-908.
81. Doghman M, Madoux F, Hodder P, Lalli E. Identification and characterization of steroidogenic factor-1 inverse agonists. Methods Enzymol. 2010;485: 3-23.
82. Madoux F, Li X, Chase P, et al. Potent, selective and cell penetrant inhibitors of SF-1 by functional ultra-high-throughput screening. Mol Pharmacol. 2008;73: 1776-1784.
83. Attar E, Tokunaga H, Imir G, et al. Prostaglandin E2 via steroidogenic factor-1 coordinately regulates transcription of steroidogenic genes necessary for estrogen synthesis in endometriosis. J Clin Endocrinol Metab. 2009;94: 623-631.
84. Jorgensen JS, Gao L. Irx3 is differentially up-regulated in female gonads during sex determination. Gene Expression Patterns. 2005; 5: 756-762.
85. Bhatt KV, Hu R, Spofford LS, Aplin AE. Mutant B-RAF signaling and cyclin D1 regulate Cks1/S-phase kinase-associated protein 2-mediated degradation of p27Kip1 in human melanoma cells. Oncogene. 2007;26: 1056-1066.
86. Lau KM, LaSpina M, Long J, Ho SM. Expression of estrogen receptor (ER)-α and ER-β in normal and malignant prostatic epithelial cells: regulation by methylation and involvement in growth regulation. Cancer Res. 2000;60: 3175-3182.