Transcription of steroidogenic acute regulatory protein in the rodent ovary and placenta: Alternative modes of cyclic adenosine 3′,5′- monophosphate dependent and independent regulation

Endocrinology

Volumn 150, Issue 2, 2009, Pages 977-989

  Yivgi Ohana, Natalie ^a   Sher, Noa ^a   Melamed Book, Naomi ^a   Eimerl, Sarah ^a   Koler, Moriah ^a   Manna, Pulak R ^b   Stocco, Douglas M ^b   Orly, Joseph ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTOR 4; CCAAT ENHANCER BINDING PROTEIN BETA; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FOLLITROPIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR GATA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE SEQUENCE; GENETIC TRANSCRIPTION; GIANT CELL; GRANULOSA CELL; HORMONE ACTION; LUTEINIZATION; MOUSE; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; TROPHOBLAST;

ANIMALS; BASE SEQUENCE; CELLS, CULTURED; CYCLIC AMP; FEMALE; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; OVARY; PHOSPHOPROTEINS; PLACENTA; PREGNANCY; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 59749087057     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0541     Document Type: Article

References (57)

1. Richards JS, Hedin L 1988 Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization. Annu Rev Physiol 50: 441-463
2. Strauss 3rd JF, Martinez F, Kiriakidou M 1996 Placental steroid hormone synthesis: uniquefeaturesandunansweredquestions. BiolReprod54:303-311
3. Miller WL 1988 Molecular biology of steroid hormone synthesis. Endocr Rev 9:295-318
4. Clark BJ, Wells J, King SR, Stocco DM 1994 The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J Biol Chem 269:28314-28322
5. Stocco DM, Sodeman TC 1991 The 30-kDa mitochondrial proteins induced by hormone stimulation in MA-10 mouse Leydig tumor cells are processed from larger precursors. J Biol Chem 266:19731-19738
6. Stocco DM, Clark BJ 1996 Regulation of the acute production of steroids in steroidogenic cells. Endocr Rev 17:221-244
7. 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
8. 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
9. Pon LA, Orme-Johnson NR 1988 Acute stimulation of corpus luteum cells by gonadotrophin or adenosine 3′,5′-monophosphate causes accumulation of a phosphoprotein concurrent with acceleration of steroid synthesis. Endocrinology 123:1942-1948
10. 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
11. 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 deducedamino acidsequenceofratP-450scc. JBiolChem264:21934-21942
12. Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP 2002 Formation of ovarian follicles during fetal development in sheep. Biol Reprod 66:1134-1150
13. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J 1998 Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072-2075
14. Silverman E, Eimerl S, Orly J 1999 CCAAT enhancer-binding protein 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
15. 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 over lapping promoter element. Mol Endocrinol 16:1864-1880
16. Sher N, Yivgi-Ohana N, Orly J 2007 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 factor-1-depen- dent gene expression in the rodent placenta and ovary. Mol Endocrinol 21:948 -962
17. Tremblay JJ, Viger RS 2001 GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 142:977-986
18. 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
19. Sher N, Orly J 2006 Analysis of trophoblast giant cell steroidogenesis in primary cultures. Methods Mol Med 122:301-31920.
20. EimerlS, OrlyJ2002Regulationofsteroidogenicgenesbyinsulin- likegrowth factor-1 and follicle-stimulating hormone: differential responses of cytochromeP450 side-chaincleavage,steroidogenicacuteregulatoryprotein,and 3β-hydroxysteroid dehydrogenase/isomerase in rat granulosa cells. Biol Re prod 67:900-910
21. 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
22. Motro B, Itin A, Sachs L, Keshet E 1990 Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis. Proc Natl Acad Sci USA 87:3092-3096
23. Mizutani T, Sonoda Y, Minegishi T, Wakabayashi K, Miyamoto K 1997 Molecular cloning, characterization and cellular distribution of rat steroidogenic acute regulatory protein (StAR) in the ovary. Life Sci 61:1497-1506
24. 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
25. Orly J, Stocco DM 1999 The role of the steroidogenic acute regulatory (StAR) protein in female reproductive tissues. Horm Metab Res 31:389-398
26. Zor T, Selinger Z 1996 Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal Biochem 236:302-308
27. Sugawara T, Holt JA, Driscoll D, Strauss 3rd JF, Lin D, Miller WL, Patterson D, Clancy KP, Hart IM, Clark BJ 1995 Human steroidogenic acute regulatory protein: functional activity in COS-1 cels, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13. Proc Natl Acad Sci USA 92:4778-4782
28. AbbaszadeI G, Arensburg J, Park CH, Kasa-VubuJ Z, Orly J, Payne AH 1997 Isolation of a new mouse βf-hydroxysteroid dehydrogenase isoform, 3 β-HSD VI, expressed during early pregnancy. Endocrinology 138:1392-1399
29. Durkee TJ, McLean MP, Hales DB, Payne AH, Waterman MR, KhanI, Gibori G 1992 P450(17α) and P450SCC gene expression and regulation in the rat placenta. Endocrinology130:1309-1317
30. 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
31. Clem BF, Clark BJ 2006 Association of the mSin3A-histone deacetylase 1/2 corepressor complex with the mouse steroidogenic acute regulatory protein gene. Mol Endocrinol 20:100-113
32. Caron KM, Ikeda Y, Soo SC, Stocco DM, Parker KL, Clark BJ 1997 Characterization of the promoter region of the mouse gene encoding the steroidogenic acute regulatory protein. Mol Endocrinol 11:138 -147
33. Manna PR, Dyson MT, Eubank DW, Clark BJ, Lalli E, Sassone-Corsi P, Zeleznik AJ, Stocco DM 2002 Regulation of steroidogenesis and the steroi- dogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol Endocrinol 16:184-199
34. Sugawara T, Kiriakidou M, McAllister JM, Kallen CB, Strauss 3rd JF 1997 Multiple steroidogenic factor 1 binding elements in the human steroidogenic acute regulatory protein gene 5′-flanking region are required for maximal promoter activity and cyclic AMP responsiveness. Biochemistry 36:7249 -7255
35. Manna PR, Wang XJ, Stocco DM 2003 Involvement of multiple transcription factors in the regulation of steroidogenic acute regulatory protein gene expression. Steroids 68:1125-1134
36. Clem BF, Hudson EA, Clark BJ 2005 Cyclic adenosine 3′,5′-monophosphate (cAMP) enhances cAMP-responsive element binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory protein gene promoter. Endocrinology 146:1348 -1356
37. Silverman E, Yivgi-Ohana N, Sher N, Bell M, Eimerl S, Orly J 2006 Transcriptional activation of the steroidogenic acute regulatory protein (StAR) gene: GATA-4 and CCAAT/enhancer-binding protein β confer synergistic responsiveness in hormone-treated rat granulosa and HEK293 cell models. Mol Cell Endocrinol 252:92-101
38. 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
39. 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
40. Sirianni R, Seely JB, Attia G, Stocco DM, CarrBR, Pezzi V, Rainey WE 2002 Liver receptor homologue-1 is expressed in human steroidogenic tissues and activates transcription of genes encoding steroidogenic enzymes. J Endocrinol 174:R13-R17
41. 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
42. 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
43. Huang N, Dardis A, Miller WL 2005 Regulation of cytochrome b5 gene transcription by Sp3, GATA-6, and steroidogenic factor 1 in human adrenal NCIH295A cells. Mol Endocrinol 19:2020-2034
44. Tremblay JJ, Viger RS 2003 Novel roles for GATA transcription factors in the regulation of steroidogenesis. JSteroid Biochem Mol Biol 85:291-298
45. LaVoie HA 2003 The role of GATA in mammalian reproduction. Exp Biol Med (Maywood) 228:1282-1290
46. 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
47. Hiroi H, Christenson LK, Chang L, Sammel MD, Berger SL, Strauss 3rd JF 2004 Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (stAR) locus associated with stAR transcription. Mol Endocrinol 18:791-806
48. Rusovici R, LaVoie HA 2003 Expression and distribution of AP-1 transcription factors in the porcine ovary. Biol Reprod 69:64-74
49. 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
50. 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
51. Goldring NB, Durica JM, Lifka J, HedinL, Ratoosh SL, Miller WL, OrlyJ, 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
52. 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
53. 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
54. Guillaumond F, Becquet D, Bosler O, Francois-Bellan AM 2002 Adrenergic inducibility of AP-1 binding in the rat pineal gland depends on prior photo- period. J Neurochem 83:157-166
55. Maronde E, Schomerus C, Stehle JH, KorfHW1997 Control of CREBphos- phorylation and its role for induction of melatonin synthesis in rat pinealocytes. Biol Cell 89:505-511
56. Reinhart AJ, Williams SC, Clark BJ, Stocco DM 1999 SF-1 (steroidogenic factor-1) and C/EBP β (CCAAT/enhancer binding proteinβ ) cooperate to regulate the murine StAR (steroidogenic acute regulatory) promoter. Mol En-docrinol 13:729-741
57. Richards JS, Ireland JJ, Rao MC, Bernath GA, Midgley JrAR, ReichertJrLE 1976 Ovarian follicular development in the rat: hormone receptor regulation by estradiol, follicle stimulating hormone and luteinizing hormone. Endocrinology 99:1562-1570