Knockdown of SF-1 and RNF31 affects components of steroidogenesis, TGFβ, and Wnt/β-catenin signaling in adrenocortical carcinoma cells

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Ehrlund, Anna ^a   Jonsson, Philip ^b   Vedin, Lise Lotte ^a   Williams, Cecilia ^b   Gustafsson, Jan Åke ^a,b   Treuter, Eckardt ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIC AMP; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN; BROXURIDINE; CARRIER PROTEIN; FORSKOLIN; RNF31 PROTEIN, HUMAN; SEX HORMONE; STEROIDOGENIC FACTOR 1;

ADRENAL CORTEX; ADRENAL CORTEX CARCINOMA; ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; GONAD DEVELOPMENT; HUMAN; HUMAN CELL; RNA INTERFERENCE; RNF31 GENE; STEREODOGENIC FACTOR 1 GENE; STEROID RELEASE; STEROIDOGENESIS; BIOLOGY; BIOSYNTHESIS; GENE SILENCING; GENETICS; METABOLISM; METHODOLOGY; MICROARRAY ANALYSIS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

ADRENAL CORTEX; ADRENOCORTICAL CARCINOMA; BETA CATENIN; BLOTTING, WESTERN; BROMODEOXYURIDINE; CARRIER PROTEINS; CELL LINE, TUMOR; COMPUTATIONAL BIOLOGY; FORSKOLIN; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GONADAL STEROID HORMONES; HUMANS; MICROARRAY ANALYSIS; POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; STEROIDOGENIC FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

EID: 84857929663     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032080     Document Type: Article

References (60)

1. Kim AC, Barlaskar FM, Heaton JH, Else T, Kelly VR, et al. (2009) In search of adrenocortical stem and progenitor cells. Endocr Rev 30: 241-263.
2. Fottner C, Hoeflich A, Wolf E, Weber MM, (2004) Role of the insulin-like growth factor system in adrenocortical growth control and carcinogenesis. Horm Metab Res 36: 397-405.
3. Wilkin F, Gagne N, Paquette J, Oligny LL, Deal C, (2000) Pediatric adrenocortical tumors: molecular events leading to insulin-like growth factor II gene overexpression. J Clin Endocrinol Metab 85: 2048-2056.
4. Figueiredo BC, Cavalli LR, Pianovski MA, Lalli E, Sandrini R, et al. (2005) Amplification of the steroidogenic factor 1 gene in childhood adrenocortical tumors. J Clin Endocrinol Metab 90: 615-619.
5. Pianovski MA, Cavalli LR, Figueiredo BC, Santos SC, Doghman M, et al. (2006) SF-1 overexpression in childhood adrenocortical tumours. Eur J Cancer 42: 1040-1043.
6. Ramayya MS, Zhou J, Kino T, Segars JH, Bondy CA, et al. (1997) Steroidogenic factor 1 messenger ribonucleic acid expression in steroidogenic and nonsteroidogenic human tissues: Northern blot and in situ hybridization studies. J Clin Endocrinol Metab 82: 1799-1806.
7. Morohashi K, Iida H, Nomura M, Hatano O, Honda S, et al. (1994) Functional difference between Ad4BP and ELP, and their distributions in steroidogenic tissues. Mol Endocrinol 8: 643-653.
8. Hanley NA, Rainey WE, Wilson DI, Ball SG, Parker KL, (2001) Expression profiles of SF-1, DAX1, and CYP17 in the human fetal adrenal gland: potential interactions in gene regulation. Mol Endocrinol 15: 57-68.
9. Hanley NA, Ball SG, Clement-Jones M, Hagan DM, Strachan T, et al. (1999) Expression of steroidogenic factor 1 and Wilms' tumour 1 during early human gonadal development and sex determination. Mech Dev 87: 175-180.
10. Luo X, Ikeda Y, Parker KL, (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77: 481-490.
11. Sadovsky Y, Crawford PA, Woodson KG, Polish JA, Clements MA, et al. (1995) 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 U S A 92: 10939-10943.
12. Schimmer BP, (2010) White PC Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol 24: 1322-1337.
13. Lalli E, (2010) Adrenocortical development and cancer: focus on SF-1. J Mol Endocrinol 44: 301-307.
14. Ehrlund A, Anthonisen EH, Gustafsson N, Venteclef N, Robertson Remen K, et al. (2009) E3 ubiquitin ligase RNF31 cooperates with DAX-1 in transcriptional repression of steroidogenesis. Mol Cell Biol 29: 2230-2242.
15. Dammer EB, Leon A, Sewer MB, (2007) Coregulator exchange and sphingosine-sensitive cooperativity of steroidogenic factor-1, general control nonderepressed 5, p54, and p160 coactivators regulate cyclic adenosine 3′,5′-monophosphate-dependent cytochrome P450c17 transcription rate. Mol Endocrinol 21: 415-438.
16. Winnay JN, Hammer GD, (2006) Adrenocorticotropic hormone-mediated signaling cascades coordinate a cyclic pattern of steroidogenic factor 1-dependent transcriptional activation. Mol Endocrinol 20: 147-166.
17. Krylova IN, Sablin EP, Moore J, Xu RX, Waitt GM, et al. (2005) Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell 120: 343-355.
18. Li Y, Choi M, Cavey G, Daugherty J, Suino K, et al. (2005) Crystallographic identification and functional characterization of phospholipids as ligands for the orphan nuclear receptor steroidogenic factor-1. Mol Cell 17: 491-502.
19. Wang W, Zhang C, Marimuthu A, Krupka HI, Tabrizizad M, et al. (2005) The crystal structures of human steroidogenic factor-1 and liver receptor homologue-1. Proc Natl Acad Sci U S A 102: 7505-7510.
20. Urs AN, Dammer E, Sewer MB, (2006) Sphingosine regulates the transcription of CYP17 by binding to steroidogenic factor-1. Endocrinology 147: 5249-5258.
21. Urs AN, Dammer E, Kelly S, Wang E, Merrill AH Jr, et al. (2007) Steroidogenic factor-1 is a sphingolipid binding protein. Mol Cell Endocrinol pp. 265-266: 174-178.
22. Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, et al. (1999) Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol Cell 3: 521-526.
23. Komatsu T, Mizusaki H, Mukai T, Ogawa H, Baba D, et al. (2004) Small ubiquitin-like modifier 1 (SUMO-1) modification of the synergy control motif of Ad4 binding protein/steroidogenic factor 1 (Ad4BP/SF-1) regulates synergistic transcription between Ad4BP/SF-1 and Sox9. Mol Endocrinol 18: 2451-2462.
24. Chen WY, Lee WC, Hsu NC, Huang F, Chung BC, (2004) SUMO modification of repression domains modulates function of nuclear receptor 5A1 (steroidogenic factor-1). J Biol Chem 279: 38730-38735.
25. Campbell LA, Faivre EJ, Show MD, Ingraham JG, Flinders J, et al. (2008) Decreased recognition of SUMO-sensitive target genes following modification of SF-1 (NR5A1). Mol Cell Biol 28: 7476-7486.
26. Yang WH, Heaton JH, Brevig H, Mukherjee S, Iniguez-Lluhi JA, et al. (2009) SUMOylation inhibits SF-1 activity by reducing CDK7-mediated serine 203 phosphorylation. Mol Cell Biol 29: 613-625.
27. Hoivik EA, Lewis AE, Aumo L, Bakke M, (2009) Molecular aspects of steroidogenic factor 1 (SF-1). Mol Cell Endocrinol 315: 27-39.
28. Vilain E, Guo W, Zhang YH, McCabe ER, (1997) DAX1 gene expression upregulated by steroidogenic factor 1 in an adrenocortical carcinoma cell line. Biochem Mol Med 61: 1-8.
29. Yu RN, Ito M, Jameson JL, (1998) The murine Dax-1 promoter is stimulated by SF-1 (steroidogenic factor-1) and inhibited by COUP-TF (chicken ovalbumin upstream promoter-transcription factor) via a composite nuclear receptor-regulatory element. Mol Endocrinol 12: 1010-1022.
30. Hoyle C, Narvaez V, Alldus G, Lovell-Badge R, Swain A, (2002) Dax1 expression is dependent on steroidogenic factor 1 in the developing gonad. Mol Endocrinol 16: 747-756.
31. Kawabe K, Shikayama T, Tsuboi H, Oka S, Oba K, et al. (1999) Dax-1 as one of the target genes of Ad4BP/SF-1. Mol Endocrinol 13: 1267-1284.
32. Manna PR, Dyson MT, Jo Y, Stocco DM, (2009) Role of dosage-sensitive sex reversal, adrenal hypoplasia congenita, critical region on the X chromosome, gene 1 in protein kinase A- and protein kinase C-mediated regulation of the steroidogenic acute regulatory protein expression in mouse Leydig tumor cells: mechanism of action. Endocrinology 150: 187-199.
33. Ding X, Lichti K, Kim I, Gonzalez FJ, Staudinger JL, (2006) Regulation of constitutive androstane receptor and its target genes by fasting, cAMP, hepatocyte nuclear factor alpha, and the coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha. J Biol Chem 281: 26540-26551.
34. Sugawara T, Sakuragi N, Minakami H, (2006) CREM confers cAMP responsiveness in human steroidogenic acute regulatory protein expression in NCI-H295R cells rather than SF-1/Ad4BP. J Endocrinol 191: 327-337.
35. Gummow BM, Winnay JN, Hammer GD, (2003) Convergence of Wnt signaling and steroidogenic factor-1 (SF-1) on transcription of the rat inhibin alpha gene. J Biol Chem 278: 26572-26579.
36. Salisbury TB, Binder AK, Grammer JC, Nilson JH, (2007) Maximal activity of the luteinizing hormone beta-subunit gene requires beta-catenin. Mol Endocrinol 21: 963-971.
37. Botrugno OA, Fayard E, Annicotte JS, Haby C, Brennan T, et al. (2004) Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation. Mol Cell 15: 499-509.
38. Kim AC, Reuter AL, Zubair M, Else T, Serecky K, et al. (2008) Targeted disruption of beta-catenin in Sf1-expressing cells impairs development and maintenance of the adrenal cortex. Development 135: 2593-2602.
39. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, et al. (2003) Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130: 3663-3670.
40. Tissier F, Cavard C, Groussin L, Perlemoine K, Fumey G, et al. (2005) Mutations of beta-catenin in adrenocortical tumors: activation of the Wnt signaling pathway is a frequent event in both benign and malignant adrenocortical tumors. Cancer Res 65: 7622-7627.
41. Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, et al. (2002) Identification of a Wnt/Dvl/beta-Catenin -& Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111: 673-685.
42. Doghman M, Cazareth J, Lalli E, (2008) The T cell factor/beta-catenin antagonist PKF115-584 inhibits proliferation of adrenocortical carcinoma cells. J Clin Endocrinol Metab 93: 3222-3225.
43. Doghman M, Cazareth J, Douguet D, Madoux F, Hodder P, et al. (2009) Inhibition of adrenocortical carcinoma cell proliferation by steroidogenic factor-1 inverse agonists. J Clin Endocrinol Metab 94: 2178-2183.
44. Liakos P, Lenz D, Bernhardt R, Feige JJ, Defaye G, (2003) Transforming growth factor beta1 inhibits aldosterone and cortisol production in the human adrenocortical cell line NCI-H295R through inhibition of CYP11B1 and CYP11B2 expression. J Endocrinol 176: 69-82.
45. Lehmann TP, Biernacka-Lukanty JM, Trzeciak WH, Li JY, (2005) Steroidogenic factor 1 gene transcription is inhibited by transforming growth factor beta. Endocr Res 31: 71-79.
46. Derebecka-Holysz N, Lehmann TP, Holysz M, Trzeciak WH, (2008) SMAD3 inhibits SF-1-dependent activation of the CYP17 promoter in H295R cells. Mol Cell Biochem 307: 65-71.
47. Massague J, (2008) TGFbeta in Cancer. Cell 134: 215-230.
48. Doghman M, Karpova T, Rodrigues GA, Arhatte M, De Moura J, et al. (2007) Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol 21: 2968-2987.
49. Logie A, Boulle N, Gaston V, Perin L, Boudou P, et al. (1999) Autocrine role of IGF-II in proliferation of human adrenocortical carcinoma NCI H295R cell line. J Mol Endocrinol 23: 23-32.
50. Zubair M, Ishihara S, Oka S, Okumura K, Morohashi K, (2006) Two-step regulation of Ad4BP/SF-1 gene transcription during fetal adrenal development: initiation by a Hox-Pbx1-Prep1 complex and maintenance via autoregulation by Ad4BP/SF-1. Mol Cell Biol 26: 4111-4121.
51. Schnabel CA, Selleri L, Cleary ML, (2003) Pbx1 is essential for adrenal development and urogenital differentiation. Genesis 37: 123-130.
52. Lichtenauer UD, Duchniewicz M, Kolanczyk M, Hoeflich A, Hahner S, et al. (2007) Pre-B-cell transcription factor 1 and steroidogenic factor 1 synergistically regulate adrenocortical growth and steroidogenesis. Endocrinology 148: 693-704.
53. de Reynies A, Assie G, Rickman DS, Tissier F, Groussin L, et al. (2009) Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 27: 1108-1115.
54. Glass CK, Saijo K, (2010) Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nat Rev Immunol 10: 365-376.
55. Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, et al. (2010) GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev 24: 381-395.
56. Edvardsson K, Strom A, Jonsson P, Gustafsson JA, Williams C, (2011) Estrogen Receptor {beta} Induces Antiinflammatory and Antitumorigenic Networks in Colon Cancer Cells. Mol Endocrinol.
57. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
58. Wettenhall JM, Smyth GK, (2004) limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706.
59. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
60. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.