Integrative analysis of SF-1 transcription factor dosage impact on genome-wide binding and gene expression regulation

Nucleic Acids Research

Volumn 41, Issue 19, 2013, Pages 8896-8907

  Doghman, Mabrouka ^a,b   Figueiredo, Bonald C ^a,c,d   Volante, Marco ^e   Papotti, Mauro ^e   Lalli, Enzo ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^d INSTITUTO DE PESQUISA PELÉ PEQUENO PRÍNCIPE   (Brazil)

^e UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NEURON RESTRICTIVE SILENCER FACTOR; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADRENAL CORTEX CELL; ARTICLE; BINDING SITE; CHROMATIN; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE REPRESSION; GENOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STEROIDOGENESIS;

ADRENAL CORTEX NEOPLASMS; BASE SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CHROMATIN; DNA; GENE DOSAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME; HUMANS; REPRESSOR PROTEINS; STEROIDOGENIC FACTOR 1;

EID: 84885971787     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt658     Document Type: Article

References (50)

1. Lala, D.S., Rice, D.A. and Parker, K.L. (1992) Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol. Endocrinol., 6, 1249-1258.
2. Morohashi, K., Honda, S., Inomata, Y., Handa, H. and Omura, T. (1992) A common transacting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J. Biol. Chem., 267, 17913-17919.
3. Parker, K.L. and Schimmer, B.P. (1997) Steroidogenic factor 1: a key determinant of endocrine development and function. Endocrine Rev., 18, 361-377.
4. Luo, X., Ikeda, Y. and Parker, K.L. (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell, 77, 481-490.
5. Sadovsky, Y., Crawford, P.A., Woodson, K.G., Polish, J.A., Clements, M.A., Tourtellotte, L.M., Simburger, K. and Milbrandt, J. (1995) Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 sidechaincleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc. Natl Acad. Sci. USA, 92, 10939-10943.
6. Zubair, M., Oka, S., Parker, K.L. and Morohashi, K. (2009) Transgenic expression of Ad4BP/SF-1 in fetal adrenal progenitor cells leads to ectopic adrenal formation. Mol. Endocrinol., 23, 1657-1667.
7. Hoivik, E.A., Lewis, A.E., Aumo, L. and Bakke, M. (2010) Molecular aspects of steroidogenic factor 1 (SF-1). Mol. Cell. Endocrinol., 315, 27-39.
8. Bland, M.L., Jamieson, C.A., Akana, S.F., Bornstein, S.R., Eisenhofer, G., Dallman, M.F. and Ingraham, H.A. (2000) Haploinsufficiency of steroidogenic factor-1 in mice disrupts adrenal development leading to an impaired stress response. Proc. Natl Acad. Sci. USA, 97, 14488-14493.
9. Beuschlein, F., Mutch, C., Bavers, D.L., Ulrich-Lai, Y.M., Engeland, W.C., Keegan, C. and Hammer, G.D. (2002) Steroidogenic factor-1 is essential for compensatory adrenal growth following unilateral adrenalectomy. Endocrinology, 143, 3122-3135.
10. Lin, L., Philibert, P., Ferraz-de-Souza, B., Kelberman, D., Homfray, T., Albanese, A., Molini, V., Sebire, N.J., Einaudi, S., Conway, G.S. et al. (2007) Heterozygous missense mutations in steroidogenic factor 1 (SF1/Ad4BP, NR5A1) are associated with 46, XY disorders of sex development with normal adrenal function. J. Clin. Endocrinol. Metab., 92, 991-999.
11. Achermann, J.C., Ozisik, G., Ito, M., Orun, U.A., Harmanci, K., Gurakan, B. and Jameson, J.L. (2002) Gonadal determination and adrenal development are regulated by the orphan nuclear receptor steroidogenic factor-1, in a dose-dependent manner. J. Clin. Endocrinol. Metab., 87, 1829-1833.
12. Doghman, M., Karpova, T., Rodrigues, G.A., Arhatte, M., De Moura, J., Cavalli, L.R., Virolle, V., Barbry, P., Zambetti, G.P., Figueiredo, B.C. et al. (2007) Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol. Endocrinol., 21, 2968-2987.
13. Pianovski, M.A., Cavalli, L.R., Figueiredo, B.C., Santos, S.C., Doghman, M., Ribeiro, R.C., Oliveira, A.G., Michalkiewicz, E., Rodrigues, G.A., Zambetti, G. et al. (2006) SF-1 overexpression in childhood adrenocortical tumours. Eur. J. Cancer, 42, 1040-1043.
14. Sbiera, S., Schmull, S., Assie, G., Voelker, H.U., Kraus, L., Beyer, M., Ragazzon, B., Beuschlein, F., Willenberg, H.S., Hahner, S. et al. (2010) High diagnostic and prognostic value of steroidogenic factor-1 expression in adrenal tumors. J. Clin. Endocrinol. Metab., 95, E161-E171.
15. Schoenherr, C.J. and Anderson, D.J. (1995) The neuron-restrictive silencer factor (NRSF) : a coordinate repressor of multiple neuron-specific genes. Science, 267, 1360-1363.
16. Chong, J.A., Tapia-Ramírez, J., Kim, S., Toledo-Aral, J.J., Zheng, Y., Boutros, M.C., Altshuller, Y.M., Frohman, M.A., Kraner, S.D. and Mandel, G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell, 80, 949-957.
17. Lee, T.I., Johnstone, S.E. and Young, R.A. (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc., 1, 729-748.
18. Ji, H., Jiang, H., Ma, W., Johnson, D.S., Myers, R.M. and Wong, W.H. (2008) An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat. Biotechnol., 26, 1293-1300.
19. Blahnik, K.R., Dou, L., O'Geen, H., McPhillips, T., Xu, X., Cao, A.R., Iyengar, S., Nicolet, C.M., Ludäscher, B., Korf, I. et al. (2010) Sole-search: an integrated analysis program for peak detection and functional annotation using ChIP-seq data. Nucleic Acids Res., 38, e13.
20. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res., 37, W202-W208.
21. Giresi, P.G. and Lieb, J.D. (2009) Isolation of active regulatory elements from eukaryotic chromatin using FAIRE (Formaldehyde Assisted Isolation of Regulatory Elements). Methods, 48, 233-239.
22. Song, L., Zhang, Z., Grasfeder, L.L., Boyle, A.P., Giresi, P.G., Lee, B.K., Sheffield, N.C., Gräf, S., Huss, M., Keefe, D. et al. (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res., 21, 1757-1767.
23. Wilson, T.E., Fahrner, T.J. and Milbrandt, J. (1993) The orphan receptors NGFI-β and steroidogenic factor 1 establish monomer binding as a third paradigm of nuclear receptor-DNA interaction. Mol. Cell. Biol., 13, 5794-5804.
24. Johnson, D.S., Mortazavi, A., Myers, R.M. and Wold, B. (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science, 316, 1497-1502.
25. Andrés, M.E., Burger, C., Peral-Rubio, M.J., Battaglioli, E., Anderson, M.E., Grimes, J., Dallman, J., Ballas, N. and Mandel, G. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl Acad. Sci. USA, 96, 9873-9878.
26. Ito, M., Achermann, J.C. and Jameson, L.J. (2000) A naturally occurring steroidogenic factor-1 mutation exhibits differential binding and activation of target genes. J. Biol. Chem., 275, 31708-31714.
27. Niwa, H., Miyazaki, J. and Smith, A.G. (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet., 24, 372-376.
28. Fowler, A.M., Solodin, N., Preisler-Mashek, M.T., Zhang, P., Lee, A.V. and Alarid, E.T. (2004) Increases in estrogen receptor-α concentration in breast cancer cells promote serine 118/104/106-independent AF-1 transactivation and growth in the absence of estrogen. FASEB J., 18, 81-93.
29. Linja, M.J., Savinainen, K.J., Saramaki, O.R., Tammela, T.L., Vessella, R.L. and Visakorpi, T. (2001) Amplification and overexpression of androgen receptor gene in hormone-refractory prostate cancer. Cancer Res., 61, 3550-3555.
30. Morohashi, K., Tsuboi-Asai, H., Matsushita, S., Suda, M., Nakashima, M., Sasano, H., Hataba, Y., Li, C.L., Fukata, J., Irie, J. et al. (1999) Structural and functional abnormalities in the spleen of an mFtz-F1 gene-disrupted mouse. Blood, 93, 1586-1594.
31. Fatchiyah., Zubair, M., Shima, Y., Oka, S., Ishihara, S., Fukui-Katoh, Y. and Morohashi, K. (2006) Differential gene dosage effects of Ad4BP/SF-1 on target tissue development. Biochem. Biophys. Res. Commun., 341, 1036-1045.
32. Lalli, E., Doghman, M., Latre de Late, P., El Wakil, A. and Mus-Veteau, I. (2013) Beyond steroidogenesis: novel target genes for SF-1 discovered by genomics. Mol. Cell. Endocrinol., 371, 154-159.
33. Ferraz-de-Souza, B., Lin, L., Shah, S., Jina, N., Hubank, M., Dattani, M.T. and Achermann, J.C. (2011) ChIP-on-chip analysis reveals angiopoietin 2 (Ang2, ANGPT2) as a novel target of steroidogenic factor-1 (SF-1, NR5A1) in the human adrenal gland. FASEB J., 25, 1166-1175.
34. Ferraz-de-Souza, B., Hudson-Davies, R.E., Lin, L., Parnaik, R., Hubank, M., Dattani, M.T. and Achermann, J.C. (2011) Sterol-Oacyltransferase 1 (SOAT1, ACAT) is a novel target of steroidogenic factor-1 (SF-1, NR5A1, Ad4BP) in the human adrenal. J. Clin. Endocrinol. Metab., 96, E663-E668.
35. Ehrlund, A., Jonsson, P., Vedin, L.L., Williams, C., Gustafsson, J.Å. and Treuter, E. (2012) Knockdown of SF-1 and RNF31 affects components of steroidogenesis, TGFβ, and Wnt/β-catenin signaling in adrenocortical carcinoma cells. PLoS One, 7, e32080.
36. Doghman, M., Arhatte, M., Thibout, H., Rodrigues, G., De Moura, J., Grosso, S., West, A.N., Laurent, M., Mas, J.-C., Bongain, A. et al. (2007) Nephroblastoma overexpressed/cysteinerich protein 61/connective tissue growth factor/nephroblastoma overexpressed gene-3 (NOV/CCN3), a selective adrenocortical cell proapoptotic factor, is down-regulated in childhood adrenocortical tumors. J. Clin. Endocrinol. Metab., 92, 3253-3260.
37. Deblois, G. and Giguère, V. (2008) Nuclear receptor location analyses in mammalian genomes: from gene regulation to regulatory networks. Mol. Endocrinol., 22, 1999-2011.
38. Rui, X., Tsao, J., Scheys, J.O., Hammer, G.D. and Schimmer, B.P. (2008) Contributions of specificity protein-1 and steroidogenic factor 1 to Adcy4 expression in Y1 mouse adrenal cells. Endocrinology, 149, 3668-3678.
39. Ye, P., Nakamura, Y., Lalli, E. and Rainey, W. (2009) Differential effects of high and low steroidogenic factor-1 expression on CYP11B2 expression and aldosterone production in adrenocortical cells. Endocrinology, 150, 1303-1309.
40. Tang, Q., Chen, Y., Meyer, C., Geistlinger, T., Lupien, M., Wang, Q., Liu, T., Zhang, Y., Brown, M. and Liu, X.S. (2011) A comprehensive view of nuclear receptor cancer cistromes. Cancer Res., 71, 6940-6947.
41. Solomon, I.H., Hager, J.M., Safi, R., McDonnell, D.P., Redinbo, M.R. and Ortlund, E.A. (2005) Crystal structure of the human LRH-1 DBD-DNA complex reveals Ftz-F1 domain positioning is required for receptor activity. J. Mol. Biol., 354, 1091-1102.
42. Little, T.H., Zhang, Y., Matulis, C.K., Weck, J., Zhang, Z., Ramachandran, A., Mayo, K.E. and Radhakrishnan, I. (2006) Sequence-specific deoxyribonucleic acid (DNA) recognition by steroidogenic factor 1: a helix at the carboxy terminus of the DNA binding domain is necessary for complex stability. Mol. Endocrinol., 20, 831-843.
43. Chen, J., Kinyamu, H.K. and Archer, T.K. (2006) Changes in attitude, changes in latitude: nuclear receptors remodeling chromatin to regulate transcription. Mol. Endocrinol., 20, 1-13.
44. Kok, F.O., Taibi, A., Wanner, S.J., Xie, X., Moravec, C.E., Love, C.E., Prince, V.E., Mumm, J.S. and Sirotkin, H.I. (2012) Zebrafish rest regulates developmental gene expression but not neurogenesis. Development, 139, 3838-3848.
45. Otto, S.J., McCorkle, S.R., Hover, J., Conaco, C., Han, J.J., Impey, S., Yochum, G.S., Dunn, J.J., Goodman, R.H. and Mandel, G. (2007) A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J. Neurosci., 27, 6729-6739.
46. Westbrook, T.F., Martin, E.S., Schlabach, M.R., Leng, Y., Liang, A.C., Feng, B., Zhao, J.J., Roberts, T.M., Mandel, G., Hannon, G.J. et al. (2005) A genetic screen for candidate tumor suppressors identifies REST. Cell, 121, 837-848.
47. Somekawa, S., Imagawa, K., Naya, N., Takemoto, Y., Onoue, K., Okayama, S., Takeda, Y., Kawata, H., Horii, M., Nakajima, T. et al. (2009) Regulation of aldosterone and cortisol production by the transcriptional repressor neuron restrictive silencer factor. Endocrinology, 150, 3110-3117.
48. Kuwahara, K., Saito, Y., Takano, M., Arai, Y., Yasuno, S., Nakagawa, Y., Takahashi, N., Adachi, Y., Takemura, G., Horie, M. et al. (2003) NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J., 22, 6310-6321.
49. Martin, D., Allagnat, F., Gesina, E., Caille, D., Gjinovci, A., Waeber, G., Meda, P. and Haefliger, J.A. (2012) Specific silencing of the REST target genes in insulin-secreting cells uncovers their participation in beta cell survival. PLoS One, 7, e45844.
50. Okamura, D., Mochizuki, K., Taniguchi, H., Tokitake, Y., Ikeda, M., Yamada, Y., Tournier, C., Yamaguchi, S., Tada, T., Schöler, H.R. et al. (2012) REST and its downstream molecule Mek5 regulate survival of primordial germ cells. Dev. Biol., 372, 190-202.