Transcriptional regulation of the cholesterol side chain cleavage cytochrome P450 gene (CYP11A1) revisited: Binding of GATA, cyclic adenosine 3′,5′-monophosphate response element-binding protein and activating protein (AP)-1 proteins to a distal novel cluster of cis-regulatory elements potentiates AP-2 and steroidogenic factor1-dependent gene expression in the rodent placenta and ovary

Molecular Endocrinology

Volumn 21, Issue 4, 2007, Pages 948-962

  Sher, Noa ^a   Yivgi Ohana, Natalie ^a   Orly, Joseph ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CIS ACTING ELEMENT; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME P450 11A1; CYTOCHROME P450 ISOENZYME; FOLLITROPIN; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR GATA 2; UNCLASSIFIED DRUG; ACTIVATING TRANSCRIPTION FACTOR 1; CELL RECEPTOR; CHOLESTEROL; CREB1 PROTEIN, MOUSE; FOSL2 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; ISOPROTEIN; SERINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE ACTIVITY; GIANT CELL; GRANULOSA CELL; LUTEINIZATION; MOUSE; NONHUMAN; OVARY FOLLICLE; OVARY FUNCTION; OVULATION; PLACENTA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TROPHOBLAST; ANIMAL; BINDING SITE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; OVARY;

RATTUS; RODENTIA;

ACTIVATING TRANSCRIPTION FACTOR 1; ANIMALS; BASE SEQUENCE; BINDING SITES; CHOLESTEROL; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; FOLLICLE STIMULATING HORMONE; FOS-RELATED ANTIGEN-2; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; MICE; MUTATION; OVARY; PLACENTA; PROMOTER REGIONS (GENETICS); PROTEIN ISOFORMS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SERINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 34247874523     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2006-0226     Document Type: Article

References (84)

1. Strauss III JF, Martinez F, Kiriakidou M 1996 Placental steroid hormone synthesis: unique features and unanswered questions. Biol Reprod 54:303-311
2. Arensburg J, Payne AH, Orly J 1999 Expression of steroidogenic genes in maternal and extraembryonic cells during early pregnancy in mice. Endocrinology 140:5220-5232
3. Schiff R, Arensburg J, Itin A, Keshet E, Orly J 1993 Expression and cellular localization of uterine side-chain cleavage cytochrome P450 messenger ribonucleic acid during early pregnancy in mice. Endocrinology 133:529-537
4. Abbaszade IG, Arensburg J, Park CH, Kasa-Vubu JZ, Orly J, Payne AH 1997 Isolation of a new mouse 3β-hydroxysteroid dehydrogenase isoform, 3-HSD VI, expressed during early pregnancy. Endocrinology 138:1392-1399
5. Bair SR, Mellon SH 2004 Deletion of the mouse P450c17 gene causes early embryonic lethality. Mol Cell Biol 24:5383-5390
6. Durkee TJ, McLean MP, Hales DB, Payne AH, Waterman MR, Khan I, Gibori G 1992 P450(17 α) and P450SCC gene expression and regulation in the rat placenta. Endocrinology 130:1309-1317
7. Yamamoto T, Chapman BM, Johnson DC, Givens CR, Mellon SH, Soares MJ 1996 Cytochrome P450 17α-hydroxylase gene expression in differentiating rat trophoblast cells. J Endocrinol 150:161-168
8. Gibori G, Khan I, Warshaw ML, McLean MP, Puryear TK, Nelson S, Durkee TJ, Azhar S, Steinschneider A, Rao MC 1988 Placental-derived regulators and the complex control of luteal cell function. Recent Prog Horm Res 44:377-429
9. Hu MC, Hsu NC, El Hadj NB, Pai CI, Chu HP, Wang CK, Chung BC 2002 Steroid deficiency syndromes in mice with targeted disruption of CYP11A1. Mol Endocrinol 16:1943-1950
10. Ben-Zimra M, Koler M, Orly J 2002 Transcription of cholesterol side-chain cleavage cytochrome P450 in the placenta: activating protein-2 assumes the role of steroidogenic factor-1 by binding to an overlapping promoter element. Mol Endocrinol 16:1864-1880
11. Auman HJ, Nottoli T, Lakiza O, Winger Q, Donaldson S, Williams T 2002 Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development 129:2733-2747
12. 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
13. 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
14. Clemens JW, Lala DS, Parker KL, Richards JS 1994 Steroidogenic factor-1 binding and transcriptional activity of the cholesterol side-chain cleavage promoter in rat granulosa cells. Endocrinology 134:1499-1508
15. Werling U, Schorle H 2002 Transcription factor gene AP-2 γ essential for early murine development. Mol Cell Biol 22:3149-3156
16. Val P, Lefrancois-Martinez AM, Veyssiere G, Martinez 2003 A SF-1 a key player in the development and differentiation of steroidogenic tissues. Nucl Recept 1:8-31
17. Chau YM, Crawford PA, Woodson KG, Polish JA, Olson LM, Sadovsky Y 1997 Role of steroidogenic-factor 1 in basal and 3′,5′-cyclic adenosine monophosphate-mediated regulation of cytochrome P450 side-chain cleavage enzyme in the mouse. Biol Reprod 57:765-771
18. Orly J, Clemens JW, Singer O, Richards JS 1996 Effects of hormones and protein kinase inhibitors on expression of steroidogenic enzyme promoters in electroporated primary rat granulosa cells. Biol Reprod 54:208-218
19. Momoi K, Waterman MR, Simpson ER, Zanger UM 1992 3′,5′-cyclic adenosine monophosphate-dependent transcription of the CYP11A (cholesterol side chain cleavage cytochrome P450) gene involves a DNA response element containing a putative binding site for transcription factor Sp1. Mol Endocrinol 6:1682-1690
20. Rice DA, Kirkman MS, Aitken LD, Mouw AR, Schimmer BP, Parker KL 1990 Analysis of the promoter region of the gene encoding mouse cholesterol side-chain cleavage enzyme. J Biol Chem 265:11713-11720
21. Ahlgren R, Simpson ER, Waterman MR, Lund J 1990 Characterization of the promoter/regulatory region of the bovine CYP11A (P-450scc) gene. Basal and cAMP-dependent expression. J Biol Chem 265:3313-3319
22. Jeyasuria P, Ikeda Y, Jamin SP, Zhao L, De Rooij DJ, Themmen AP, Behringer RR, Parker KL 2004 Cell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol 18:1610-1619
23. Liu Z, Simpson ER 1997 Steroidogenic factor 1 (SF-1) and SP1 are required for regulation of bovine CYP11A gene expression in bovine luteal cells and adrenal Y1 cells. Mol Endocrinol 11:127-137
24. Shi D, Kellems RE 1998 Transcription factor AP-2γ regulates murine adenosine deaminase gene expression during placental development. J Biol Chem 273:27331-27338
25. Guo IC, Tsai HM, Chung BC 1994 Actions of two different cAMP-responsive sequences and an enhancer of the human CYP11A1 (P450scc) gene in adrenal Y1 and placental JEG-3 cells. J Biol Chem 269:6362-6369
26. Carlone DL, Richards JS 1997 Functional interactions, phosphorylation, and levels of 3′,5′-cyclic adenosine monophosphate-regulatory element binding protein and steroidogenic factor-1 mediate hormone-regulated and constitutive expression of aromatase in gonadal cells. Mol Endocrinol 11:292-304
27. Falender AE, Lanz R, Malenfant D, Belanger L, Richards JS 2003 Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. Endocrinology 144:3598-3610
28. Hinshelwood MM, Repa JJ, Shelton JM, Richardson JA, Mangelsdorf DJ, Mendelson CR 2003 Expression of LRH-1 and SF-1 in the mouse ovary: localization in different cell types correlates with differing function. Mol Cell Endocrinol 207:39-45
29. Jimenez P, Saner K, Mayhew B, Rainey WE 2003 GATA-6 is expressed in the human adrenal and regulates transcription of genes required for adrenal androgen biosynthesis. Endocrinology 144:4285-4288
30. Nulsen JC, Silavin SL, Kao LC, Ringler GE, Kliman HJ, Strauss JF, 3rd 1989 Control of the steroidogenic machinery of the human trophoblast by cyclic AMP. J Reprod Fertil Suppl 37:147-153
31. Yamamoto T, Chapman BM, Clemens JW, Richards JS, Soares MJ 1995 Analysis of cytochrome P-450 side-chain cleavage gene promoter activation during trophoblast cell differentiation. Mol Cell Endocrinol 113:183-194
32. Ringler GE, Kao LC, Miller WL, Strauss III JF 1989 Effects of 8-bromo-cAMP on expression of endocrine functions by cultured human trophoblast cells. Regulation of specific mRNAs. Mol Cell Endocrinol 61:13-21
33. Richards JS, Hedin L 1988 Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization. Annu Rev Physiol 50:441-463
34. Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK, Sharma SC 2002 Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 57:195-220
35. Eimerl S, Orly J 2002 Regulation of steroidogenic genes by insulin-like growth factor-1 and follicle-stimulating hormone: differential responses of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, and 3β-hydroxysteroid dehydrogenase/isomerase in rat granulosa cells. Biol Reprod 67:900-910
36. Silverman E, Eimerl S, Orly J 1999 CCAAT enhancer-binding protein β and GATA-4 binding regions within the promoter of the steroidogenic acute regulatory protein (StAR) gene are required for transcription in rat ovarian cells. J Biol Chem 274:17987-17996
37. Muchardt C, Li C, Kornuc M, Gaynor R 1990 CREB regulation of cellular cyclic AMP-responsive and adenovirus early promoters. J Virol 64:4296-4305
38. Manna PR, Eubank DW, Stocco DM 2004 Assessment of the role of activator protein-1 on transcription of the mouse steroidogenic acute regulatory protein gene. Mol Endocrinol 18:558-573
39. Coss D, Jacobs SB, Bender CE, Mellon PL 2004 A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone β gene by gonadotropin-releasing hormone. J Biol Chem 279:152-162
40. Rim JS, Kozak LP 2002 Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene. J Biol Chem 277:34589-34600
41. Tremblay JJ, Robert NM, Viger RS 2001 Modulation of endogenous GATA-4 activity reveals its dual contribution to Mullerian inhibiting substance gene transcription in Sertoli cells. Mol Endocrinol 15:1636-1650
42. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C 1998 A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18:967-977
43. Lamas M, Sassone-Corsi P 1997 The dynamics of the transcriptional response to cyclic adenosine 3′,5′-monophosphate: recurrent inducibility and refractory phase. Mol Endocrinol 11:1415-1424
44. Olive M, Krylov D, Echlin DR, Gardner K, Taparowsky E, Vinson C 1997 A dominant negative to activation protein-1 (AP1) that abolishes DNA binding and inhibits oncogenesis. J Biol Chem 272:18586-18594
45. Sadovsky Y, Dorn C 2000 Function of steroidogenic factor 1 during development and differentiation of the reproductive system. Rev Reprod 5:136-142
46. Hu MC, Hsu NC, Pai CI, Wang CK, Chung B 2001 Functions of the upstream and proximal steroidogenic factor 1 (SF-1)-binding sites in the CYP11A1 promoter in basal transcription and hormonal response. Mol Endocrinol 15:812-818
47. 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
48. Guo IC, Hu MC, Chung BC 2003 Transcriptional regulation of CYP11A1. J Biomed Sci 10:593-598
49. Huang N, Miller WL 2000 Cloning of factors related to HIV-inducible LBP proteins that regulate steroidogenic factor-1-independent human placental transcription of the cholesterol side-chain cleavage enzyme, P450scc. J Biol Chem 275:2852-2858
50. Huang N, Miller WL 2005 LBP proteins modulate SF1-independent expression of P450scc in human placental JEG-3 cells. Mol Endocrinol 19:409-420
51. Tevosian SG, Albrecht KH, Crispino JD, Fujiwara Y, Eicher EM, Orkin SH 2002 Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 129:4627-4634
52. Tremblay JJ, Viger RS 2001 GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 142:977-986
53. Robert NM, Tremblay JJ, Viger RS 2002 Friend of GATA (FOG)-1 and FOG-2 differentially repress the GATA-dependent activity of multiple gonadal promoters. Endocrinology 143:3963-3973
54. Fluck CE, Miller WL 2004 GATA-4 and GATA-6 modulate tissue-specific transcription of the human gene for P450c17 by direct interaction with Sp1. Mol Endocrinol 18:1144-1157
55. Martin LJ, Taniguchi H, Robert NM, Simard J, Tremblay JJ, Viger RS 2005 Gata factors and the nuclear receptors Sf-1/Lrh-1 are key mutual partners in the regulation of the human Hsd3β2 promoter. Mol Endocrinol 19:2358-2370
56. Huang N, Dardis A, Miller WL 2005 Regulation of cytochrome b5 gene transcription by Sp3, GATA-6, and steroidogenic factor 1 in human adrenal NCI-H295A Cells. Mol Endocrinol 19:2020-2034
57. Tremblay JJ, Viger RS 2003 Novel roles for GATA transcription factors in the regulation of steroidogenesis. J Steroid Biochem Mol Biol 85:291-298
58. Ma GT, Roth ME, Groskopf JC, Tsai FY, Orkin SH, Grosveld F, Engel JD, Linzer DI 1997 GATA-2 and GATA-3 regulate trophoblast-specific gene expression in vivo. Development 124:907-914
59. LaVoie HA 2003 The role of GATA in mammalian reproduction. Exp Biol Med (Maywood) 228:1282-1290
60. Heikinheimo M, Ermolaeva M, Bielinska M, Rahman NA, Narita N, Huhtaniemi IT, Tapanainen JS, Wilson DB 1997 Expression and hormonal regulation of transcription factors GATA-4 and GATA-6 in the mouse ovary. Endocrinology 138:3505-3514
61. Ko LJ, Engel JD 1993 DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol 13:4011-4022
62. Ma GT, Linzer DI 2000 GATA-2 restricts prolactin-like protein A expression to secondary trophoblast giant cells in the mouse. Biol Reprod 63:570-574
63. Cooke BA 1999 Signal transduction involving cyclic AMP-dependent and cyclic AMP-independent mechanisms in the control of steroidogenesis. Mol Cell Endocrinol 151:25-35
64. Richards JS 2001 New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 15:209-218
65. Inoue H, Watanabe N, Higashi Y, Fujii-Kuriyama Y 1991 Structures of regulatory regions in the human cytochrome P-450scc (desmolase) gene. Eur J Biochem 195:563-569
66. Doi J, Takemori H, Lin XZ, Horike N, Katoh Y, Okamoto M 2002 Salt-inducible kinase represses cAMP-dependent protein kinase-mediated activation of human cholesterol side chain cleavage cytochrome P450 promoter through the CREB basic leucine zipper domain. J Biol Chem 277:15629-15637
67. Martinez F, Kiriakidou M, Strauss III JF 1997 Structural and functional changes in mitochondria associated with trophoblast differentiation: methods to isolate enriched preparations of syncytiotrophoblast mitochondria. Endocrinology 138:2172-2183
68. Watanabe N, Inoue H, Fujii-Kuriyama Y 1994 Regulatory mechanisms of cAMP-dependent and cell-specific expression of human steroidogenic cytochrome P450scc (CYP11A1) gene. Eur J Biochem 222:825-834
69. Sharma SC, Richards JS 2000 Regulation of AP1 (Jun/Fos) factor expression and activation in ovarian granulosa cells. Relation of JunD and Fra2 to terminal differentiation. J Biol Chem 275:33718-33728
70. Mukherjee A, Park-Sarge OK, Mayo KE 1996 Gonadotropins induce rapid phosphorylation of the 3′,5′-cyclic adenosine monophosphate response element binding protein in ovarian granulosa cells. Endocrinology 137:3234-3245
71. Gonzalez-Robayna IJ, Alliston TN, Buse P, Firestone GL, Richards JS 1999 Functional and subcellular changes in the A-kinase-signaling pathway: relation to aromatase and Sgk expression during the transition of granulosa cells to luteal cells. Mol Endocrinol 13:1318-1337
72. Oonk RB, Krasnow JS, Beattie WG, Richards JS 1989 Cyclic AMP-dependent and -independent regulation of cholesterol side chain cleavage cytochrome P-450 (P-450scc) in rat ovarian granulosa cells and corpora lutea. cDNA and deduced amino acid sequence of rat P-450scc. J Biol Chem 264:21934-21942
73. Goldring NB, Durica JM, Lifka J, Hedin L, Ratoosh SL, Miller WL, Orly J, Richards JS 1987 Cholesterol side-chain cleavage P450 messenger ribonucleic acid: evidence for hormonal regulation in rat ovarian follicles and constitutive expression in corpora lutea. Endocrinology 120:1942-1950
74. Maronde E, Schomerus C, Stehle JH, Korf HW 1997 Control of CREB phosphorylation and its role for induction of melatonin synthesis in rat pinealocytes. Biol Cell 89:505-511
75. Guillaumond F, Becquet D, Bosler O, Francois-Bellan AM 2002 Adrenergic inducibility of AP-1 binding in the rat pineal gland depends on prior photoperiod. J Neurochem 83:157-166
76. Trocme C, Ravassard P, Sassone-Corsi P, Mallet J, Biguet NF 2001 CREM and ICER are differentially implicated in trans-synaptic induction of tyrosine hydroxylase gene expression in adrenal medulla and sympathetic ganglia of rat. J Neurosci Res 65:91-99
77. Tkach V, Tulchinsky E, Lukanidin E, Vinson C, Bock E, Berezin V 2003 Role of the Fos family members, c-Fos, Fra-1 and Fra-2, in the regulation of cell motility. Oncogene 22:5045-5054
78. Sher N, Orly J 2006 Analysis of trophoblast giant cell steroidogenesis in primary cultures. Methods Mol Med 122:301-319
79. Russell DL, Doyle KM, Gonzales-Robayna I, Pipaon C, Richards JS 2003 Egr-1 induction in rat granulosa cells by follicle-stimulating hormone and luteinizing hormone: combinatorial regulation by transcription factors cyclic adenosine 3′,5′-monophosphate regulatory element binding protein, serum response factor, sp1, and early growth response factor-1. Mol Endocrinol 17:520-533
80. Sriraman V, Sharma SC, Richards JS 2003 Transactivation of the progesterone receptor gene in granulosa cells: evidence that Sp1/Sp3 binding sites in the proximal promoter play a key role in luteinizing hormone inducibility. Mol Endocrinol 17:436-449
81. Orly J, Sato G, Erickson GF 1980 Serum suppresses the expression of hormonally induced functions in cultured granulosa cells. Cell 20:817-827
82. Zor T, Selinger Z 1996 Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal Biochem 236:302-308
83. Knofler M, Saleh L, Bauer S, Vasicek R, Griesinger G, Strohmer H, Helmer H, Husslein P 2000 Promoter elements and transcription factors involved in differentiation-dependent human chorionic gonadotrophin-α messenger ribonucleic acid expression of term villous trophoblasts. Endocrinology 141:3737-3748
84. Ronen-Fuhrmann T, Timberg R, King SR, Hales KH, Hales DB, Stocco DM, Orly J 1998 Spatio-temporal expression patterns of steroidogenic acute regulatory protein (StAR) during follicular development in the rat ovary. Endocrinology 139:303-315