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

Molecular Endocrinology

Volumn 18, Issue 10, 2004, Pages 2451-2462

  Komatsu, Tomoko ^a,b   Mizusaki, Hirofumi ^a,c   Mukai, Tokuo ^a   Ogawa, Hidesato ^a   Baba, Daichi ^d   Shirakawa, Masahiro ^d   Hatakeyama, Shigetsugu ^c,e   Nakayama, Keiichi I ^c,e   Yamamoto, Hideki ^f   Kikuchi, Akira ^f   Morohashi, Ken Ichirou ^a,b,c  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

^f HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LYSINE; STEROIDOGENIC FACTOR 1; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; WT1 PROTEIN;

ARTICLE; BINDING SITE; CELL CULTURE; EMBRYO CELL; HUMAN; HUMAN CELL; KIDNEY CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN MOTIF; REACTION ANALYSIS; STEROIDOGENESIS; SYNERGY CONTROL MOTIF; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; CELL LINE; DNA-BINDING PROTEINS; HIGH MOBILITY GROUP PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; PLASMIDS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SUMO-1 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 5044236130     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0173     Document Type: Article

References (60)

1. Morohashi K, Honda S, Inomata Y, Handa H, Omura T 1992 A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J Biol Chem 267:17913-17919
2. Lala DS, Rice DA, Parker KL 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
3. 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
4. Sadovsky Y, Crawford PA, Woodson KG, Polish JA, Clements MA, Tourtellotte LM, Simburger K, Milbrandt J 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 USA 92:10939-10943
5. Shinoda K, Lei H, Yoshii H, Nomura M, Nagano M, Shiba H, Sasaki H, Osawa Y, Ninomiya Y, Niwa O, Morohashi K, Li E 1995 Developmental defects of the ventromedial hypothalamic nucleus and pituitary gonadotroph in the Ftz-F1 disrupted mice. Dev Dyn 204:22-29
6. Morohashi K, Tsuboi-Asai H, Matsushita S, Suda M, Nakashima M, Sasano H, Hataba Y, Li CL, Fukata J, Irie J, Watanabe T, Nagura H, Li E 1999 Structural and functional abnormalities in the spleen of an mFtz-F1 gene-disrupted mouse. Blood 93:1586-1594
7. Crawford PA, Polish JA, Ganpule G, Sadovsky Y 1997 The activation function-2 hexamer of steroidogenic factor-1 is required, but not sufficient for potentiation by SRC-1. Mol Endocrinol 11:1626-1635
8. Ito M, Yu RN, Jameson JL 1998 Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol Endocrinol 12:290-301
9. Monte D, DeWitte F, Hum DW 1998 Regulation of the human P450scc gene by steroidogenic factor 1 is mediated by CBP/p300. J Biol Chem 273:4585-4591
10. Borud B, Hoang T, Bakke M, Jacob AL, Lund J, Mellgren G 2002 The nuclear receptor coactivators p300/CBP/cointegrator-associated protein (p/CIP) and transcription intermediary factor 2 (TIF2) differentially regulate PKA-stimulated transcriptional activity of steroidogenic factor 1. Mol Endocrinol 16:757-773
11. Crawford PA, Dorn C, Sadovsky Y, Milbrandt J 1998 Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 18:2949-2956
12. Mizusaki H, Kawabe K, Mukai T, Ariyoshi E, Kasahara M, Yoshioka H, Swain A, Morohashi K 2003 Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol Endocrinol 17:507-519
13. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P 1998 Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 18: 6653-6665
14. Tremblay JJ, Viger RS 1999 Transcription factor GATA-4 enhances Mullerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol Endocrinol 13:1388-1401
15. Nachtigal MW, Hirokawa Y, Enyeart-VanHouten DL, Flanagan JN, Hammer GD, Ingraham HA 1998 Wilms' tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93:445-454
16. Hossain A, Saunders GF 2003 Role of Wilms tumor 1 (WT1) in the transcriptional regulation of the Mullerian-inhibiting substance promoter. Biol Reprod 69: 1808-1814
17. Tremblay JJ, Marcil A, Gauthier Y, Drouin J 1999 Ptx1 regulates SF-1 activity by an interaction that mimics the role of the ligand-binding domain. EMBO J 18:3431-3441
18. Kabe Y, Goto M, Shima D, Imai T, Wada T, Morohashi K, Shirakawa M, Hirose S, Handa H 1999 The role of human MBF1 as a transcriptional coactivator. J Biol Chem 274: 34196-34202
19. Halvorson LM, Ito M, Jameson JL, Chin WW 1998 Steroidogenic factor-1 and early growth response protein 1 act through two composite DNA binding sites to regulate luteinizing hormone β-subunit gene expression. J Biol Chem 273:14712-14720
20. Dorn C, Ou Q, Svaren J, Crawford PA, Sadovsky Y 1999 Activation of luteinizing hormone β gene by gonadotropin-releasing hormone requires the synergy of early growth response-1 and steroidogenic factor-1. J Biol Chem 274:13870-13876
21. Gizard F, Lavallee B, DeWitte F, Teissier E, Staels B, Hum DW 2002 The transcriptional regulating protein of 132 kDa (TReP-132) enhances P450scc gene transcription through interaction with steroidogenic factor-1 in human adrenal cells. J Biol Chem 277:39144-39155
22. Ito M, Yu R, Jameson JL 1997 DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol Cell Biol 17:1476-1483
23. Ou Q, Mouillet JF, Yan X, Dorn C, Crawford PA, Sadovsky Y 2001 The DEAD box protein DP103 is a regulator of steroidogenic factor-1. Mol Endocrinol 15:69-79
24. Jorgensen JS, Nilson JH 2001 AR suppresses transcription of the LHβ subunit by interacting with steroidogenic factor-1. Mol Endocrinol 15:1505-1516
25. Mukai T, Kusaka M, Kawabe K, Goto K, Nawata H, Fujieda K, Morohashi K 2002 Sexually dimorphic expression of Dax-1 in the adrenal cortex. Genes Cells 7:717-729
26. Borud B, Mellgren G, Lund J, Bakke M 2003 Cloning and characterization of a novel zinc finger protein that modulates the transcriptional activity of nuclear receptors. Mol Endocrinol 17:2303-2319
27. Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, Weigel NL, Ingraham HA 1999 Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol Cell 3:521-526
28. Desclozeaux M, Krylova IN, Horn F, Fletterick RJ, Ingraham HA 2002 Phosphorylation and intramolecular stabilization of the ligand binding domain in the nuclear receptor steroidogenic factor 1. Mol Cell Biol 22:7193-7203
29. Sewer MB, Waterman MR 2003 CAMP-dependent protein kinase enhances CYP17 transcription via MKP-1 activation in H295R human adrenocortical cells. J Biol Chem 278:8106-8111
30. Jacob AL, Lund J, Martinez P, Hedin L 2001 Acetylation of steroidogenic factor 1 protein regulates its transcriptional activity and recruits the coactivator GCN5. J Biol Chem 276:37659-37664
31. Melchior F 2000 SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol 16:591-626
32. Muller S, Hoege C, Pyrowolakis G, Jentsch S 2001 SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol 2:202-210
33. Seeler JS, Dejean A 2003 Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 4:690-699
34. Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, Snowden AW, Garcia-Wilson E, Perkins ND, Hay RT 2003 P300 transcriptional repression is mediated by SUMO modification. Mol Cell 11:1043-1054
35. Lin X, Sun B, Liang M, Liang YY, Gast A, Hildebrand J, Brunicardi FC, Melchior F, Feng XH 2003 Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol Cell 11:1389-1396
36. Ross S, Best JL, Zon LI, Gill G 2002 SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol Cell 10:831-842
37. Desterro JM, Rodriguez MS, Hay RT 1998 SUMO-1 modification of IκBα inhibits NF-κB activation. Mol Cell 2:233-239
38. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S 2002 RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141
39. Verger A, Perdomo J, Crossley M 2003 Modification with SUMO. A role in transcriptional regulation. EMBO Rep 4:137-142
40. Gill G 2003 Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr Opin Genet Dev 13:108-113
41. Iniguez-Lluhi JA, Pearce D 2000 A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol Cell Biol 20:6040-6050
42. Subramanian L, Benson MD, Iniguez-Lluhi JA 2003 A synergy control motif within the attenuator domain of CCAAT/enhancer-binding protein α inhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J Biol Chem 278:9134-9141
43. Holmstrom S, Van Antwerp ME, Iniguez-Lluhi JA 2003 Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc Natl Acad Sci USA 100:15758-15763
44. Duval D, Duval G, Kedinger C, Poch O, Boeuf H 2003 The 'PINIT' motif, of a newly identified conserved domain of the PIAS protein family, is essential for nuclear retention of PIAS3L. FEBS Lett 554:111-118
45. Honda S, Morohashi K, Nomura M, Takeya H, Kitajima M, Omura T 1993 Ad4BP regulating steroidogenic P-450 gene is a member of steroid hormone receptor superfamily. J Biol Chem 268:7494-7502
46. Ueda H, Sun GC, Murata T, Hirose S 1992 A novel DNA-binding motif abuts the zinc finger domain of insect nuclear hormone receptor FTZ-F1 and mouse embryonal long terminal repeat-binding protein. Mol Cell Biol 12: 5667-5672
47. Li LA, Chiang EF, Chen JC, Hsu NC, Chen YJ, Chung BC 1999 Function of steroidogenic factor 1 domains in nuclear localization, transactivation, and interaction with transcription factor TFIIB and c-Jun. Mol Endocrinol 13: 1588-1598
48. Bies J, Markus J, Wolff L 2002 Covalent attachment of the SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity. J Biol Chem 277:8999-9009
49. Bhaskar V, Smith M, Courey AJ 2002 Conjugation of Smt3 to dorsal may potentiate the Drosophila immune response. Mol Cell Biol 22:492-504
50. Pearce D, Matsui W, Miner JN, Yamamoto KR 1998 Glucocorticoid receptor transcriptional activity determined by spacing of receptor and nonreceptor DNA sites. J Biol Chem 273:30081-30085
51. Yang SH, Jaffray E, Hay RT, Sharrocks AD 2003 Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity. Mol Cell 12:63-74
52. Yang SH, Sharrocks AD 2004 SUMO promotes HDAC-mediated transcriptional repression. Mol Cell 13:611-617
53. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R 2001 PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15:3088-3103
54. Schmidt D, Muller S 2002 Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci USA 99:2872-2877
55. Long J, Matsuura I, He D, Wang G, Shuai K, Liu F 2003 Repression of Smad transcriptional activity by PIASy, an inhibitor of activated STAT. Proc Natl Acad Sci USA 100:9791-9796
56. Tussie-Luna MI, Bayarsaihan D, Seto E, Ruddle FH, Roy AL 2002 Physical and functional interactions of histone deacetylase 3 with TFII-I family proteins and PIASxβ. Proc Natl Acad Sci USA 99:12807-12812
57. Umesono K, Murakami KK, Thompson CC, Evans RM 1991 Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 65:1255-1266
58. Haber DA, Sohn RL, Buckler AJ, Pelletier J, Call KM, Housman DE 1991 Alternative splicing and genomic structure of the Wilms tumor gene WT1. Proc Natl Acad Sci USA 88:9618-9622
59. Morohashi K, Zanger UM, Honda S, Hara M, Waterman MR, Omura T 1993 Activation of CYP11A and CYP11B gene promoters by the steroidogenic cell-specific transcription factor, Ad4BP. Mol Endocrinol 7:1196-1204
60. Chen WY, Lee WC, Hsu NC, Huang F, Chung BC 10 June 2004 SUMO modification of repression domains modulates function of nuclear receptor 5A1 (steroidogenic factor-1). J Biol Chem 10.1074/jbc.M405006200