Protein kinase A-dependent cooperation between GATA and CCAAT/enhancer-binding protein transcription factors regulates steroidogenic acute regulatory protein promoter activity

Endocrinology

Volumn 143, Issue 10, 2002, Pages 3935-3945

  Tremblay, Jacques J ^a   Hamel, Frédéric ^a   Viger, Robert S ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT BINDING FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR GATA 1;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL COMPARTMENTALIZATION; CHOLESTEROL TRANSPORT; GENE EXPRESSION REGULATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA; DNA-BINDING PROTEINS; GATA4 TRANSCRIPTION FACTOR; MICE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 0036773219     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2002-220413     Document Type: Article

References (73)

1. Orkin SH 1992 GATA-binding transcription factors in hematopoietic cells. Blood 80:575-581
2. Molkentin JD 2000 The zinc finger-containing transcription factors GATA-4, -5,and-6. Ubiquitously expressed regulators of tissue-specific gene expression. J Biol Chem 275:38949-38952
3. Weiss MJ, Orkin SH 1995 GATA transcription factors: Key regulators of hematopoiesis. Exp Hematol 23:99-107
4. Simon MC 1995 Gotta have GATA. Nat Genet 11:9-11
5. Orkin SH 1998 Embryonic stem cells and transgenic mice in the study of hematopoiesis. Int J Dev Biol 42:927-934
6. Charron F, Nemer M 1999 GATA transcription factors and cardiac development. Semin Cell Dev Biol 10:85-91
7. Tong Q, Dalgin G, Xu H, Ting CN, Leiden JM, Hotamisligil GS 2000 Function of GATA transcription factors in preadipocyte-adipocyte transition. Science 290:134-138
8. Nichols KE, Crispino JD, Poncz M, White JG, Orkin SH, Maris JM, Weiss MJ 2000 Familial dyserythropoietic anaemia and thrombocytopenia due to an inherited mutation in GATA-1. Nat Genet 24:266-270
9. Van Esch H, Groenen P, Nesbit MA, Schuffenhauer S, Lichtner P, Vanderlinden G, Hardling B, Beetz R, Bilous RW, Holdaway I, Shaw NJ, Fryns J-P, Van de Ven W, Thakker R, Devriendt K 2000 GATA-3 haplo-insufficiency causes human HDR syndrome. Nature 406:419-422
10. Maeda M, Kubo K, Nishi T, Futai M 1996 Roles of gastric GATA DNA-binding proteins. J Exp Biol 199:513-520
11. Rosenfeld MG, Briata P, Dasen J, Gleiberman AS, Kioussi C, Lin C, O'Connell SM, Ryan A, Szeto DP, Treier M 2000 Multistep signaling and transcriptional requirements for pituitary organogenesis in vivo. Recent Prog Horm Res 55:1-13
12. Nardelli J, Thiesson D, Fujiwara Y, Tsai FY, Orkin SH 1999 Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev Biol 210:305-321
13. Viger RS, Mertineit C, Trasler JM, Nemer M 1998 Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Müllerian inhibiting substance promoter. Development 125:2665-2675
14. Kiiveri S, Siltanen S, Rahman N, Bielinska M, Lehto VP, Huhtaniemi IT, Muglia LJ, Wilson DB, Heikinheimo M 1999 Reciprocal changes in the expression of transcription factors GATA-4 and GATA-6 accompany adrenocortical tumorigenesis in mice and humans. Mol Med 5:490-501
15. Heikinheimo M, Ermolaeva M, Bielinska M, Rahnman 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
16. Laitinen MP, Anttonen M, Ketola I, Wilson DB, Ritvos O, Butzow R, Heikinheimo M 2000 Transcription factors GATA-4 and GATA-6 and a GATA family cofactor, FOG-2, are expressed in human ovary and sex cord-derived ovarian tumors. J Clin Endocrinol Metab 85:3476-3483
17. Ketola I, Rahman N, Toppari J, Bielinska M, Porter-Tinge SB, Tapanainen JS, Huhtaniemi IT, Wilson DB, Heikinheimo M 1999 Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 140:1470-1480
18. Ketola I, Pentikainen V, Vaskivuo T, Ilvesmaki V, Herva R, Dunkel L, Tapanainen JS, Toppari J, Heikinheimo M 2000 Expression of transcription factor GATA-4 during human testicular development and disease. J Clin Endocrinol Metab 85:3925-3931
19. McCoard SA, Wise TH, Fahrenkrug SC, Ford JJ 2001 Temporal and spatial localization patterns of GATA-4 during porcine gonadogenesis. Biol Reprod 65:366-374
20. Tremblay JJ, Viger RS 2001 GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 142:977-986
21. 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
22. Wooton-Kee CR, Clark BJ 2000 Steroidogenic factor-1 influences protein-deoxyribonucleic acid interactions within the cyclic adenosine 3, 5-monophosphate-responsive regions of the murine steroidogenic acute regulatory protein gene. Endocrinology 141:1345-1355
23. Stocco DM 2001 StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 63:193-213
24. Piao YS, Peltoketo H, Vihko P, Vihko R 1997 The proximal promoter region of the gene encoding human 17β-hydroxysteroid dehydrogenase type I contains GATA, AP-2, and Sp1 response elements: Analysis of promoter function in choriocarcinoma cells. Endocrinology 138:3417-3425
25. 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
26. Caron KM, Soo SC, Wetsel WC, Stocco DM, Clark BJ, Parker KL 1997 Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia. Proc Natl Acad Sci USA 94:11540-11545
27. Hasegawa T, Zhao L, Caron KM, Majdic G, Suzuki T, Shizawa S, Sasano H, Parker KL 2000 Developmental roles of the steroidogenic acute regulatory protein (STAR) as revealed by StAR knockout mice. Mol Endocrinol 14:1462-1471
28. Clark BJ, Soo SC, Caron KM, Ikeda Y, Parker KL, Stocco DM 1995 Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol Endocrinol 9:1346-1355
29. Clark BJ, Combs R, Hales KH, Hales DB, Stocco DM 1997 Inhibition of transcription affects synthesis of steroidogenic acute regulatory protein and steroidogenesis in MA-10 mouse Leydig tumor cells. Endocrinology 138:4893-4901
30. Manna PR, Dyson MT, Eubank DW, Clark BJ, Lalli E, Sassone-Corsi P, Zeleznik AJ, Stocco DM 2002 Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol Endocrinol 16:184-199
31. 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
32. Sugawara T, Holt JA, Kiriakidou M, Strauss III JF 1996 Steroidogenic factor 1-dependent promoter activity of the human steroidogenic acute regulatory protein (STAR) gene. Biochemistry 35:9052-9059.
33. Clark BJ, Combs R 1999 Angiotensin II and cyclic adenosine 3′,5′-monophosphate induce human steroidogenic acute regulatory protein transcription through a common steroidogenic factor-1 element. Endocrinology 140:4390-4398
34. Christenson LK, Johnson PF, McAllister JM, Strauss III JF 1999 CCAAT/enhancer-binding proteins regulate expression of the human steroidogenic acute regulatory protein (STAR) gene. J Biol Chem 274:26591-26598.
35. Nalbant D, Williams SC, Stocco DM, Khan SA 1998 Luteinizing hormone-dependent gene regulation in Leydig cells may be mediated by CCAAT/enhancer-binding protein-β. Endocrinology 139:272-279
36. Tremblay JJ, Viger RS 1999 Transcription factor GATA-4 enhances Müllerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol Endocrinol 13:1388-1401
37. Tremblay JJ, Robert NM, Viger RS 2001 Modulation of endogenous GATA-4 activity reveals its dual contribution to Müllerian inhibiting substance gene transcription in Sertoli cells. Mol Endocrinol 15:1636-1650
38. Lala DS, Rice DA, Parker KL 1992 Steroidogenic factor 1, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol Endocrinol 6:1249-1258
39. Lu JR, McKinsey A, Xu H, Wang DZ, Richardson JA, Olson EN 1999 FOG-2, a heart- and brain-enriched cofactor for GATA transcription factors. Mol Cell Biol 19:4495-4502
40. Mayr B, Montminy M 2001 Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599-609
41. van Patten SM, Howard P, Walsh DA, Maurer RA 1992 The α- and β-isoforms of the inhibitor protein of the 3′,5′-cyclic adenosine monophosphate-dependent protein kinase: Characteristics and tissue- and developmental-specific expression. Mol Endocrinol 6:2114-2122
42. Cao Z, Umek RM, McKnight SL 1991 Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 5:1538-1552
43. Ascoli M 1981 Characterization of several clonal lines of cultured Leydig tumor cells: Gonadotropin receptors and steroidogenic responses. Endocrinology 108:88-95
44. Schreiber E, Matthias P, Muller MM, Schaffner W 1989 Rapid detection of octamer binding proteins with 'mini-extracts,' prepared from a small number of cells. Nucleic Acids Res 17:6419
45. Wang X, Walsh LP, Reinhart AJ, Stocco DM 2000 The role of arachidonic acid in steroidogenesis and steroidogenic acute regulatory (STAR) gene and protein expression. J Biol Chem 275:20204-20209
46. Tsang AP, Visvader JE, Turner CA, Fujiwara Y, Yu C, Weiss MJ, Crossley M, Orkin SH 1997 FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 90:109-119
47. Tevosian SG, Deconinck AE, Cantor AB, Rieff HI, Fujiwara Y, Corfas G, Orkin SH 1999 FOG-2: A novel GATA-family cofactor related to multitype zinc-finger proteins Friend of GATA-1 and U-shaped. Proc Natl Acad Sci USA 96:950-955
48. Fox AH, Liew C, Holmes M, Kowalski K, Mackay J, Crossley M 1999 Transcriptional cofactors of the FOG family interact with GATA proteins by means of multiple zinc fingers. EMBO J 18:2812-2822
49. Svensson EC, Tufts RL, Polk CE, Leiden JM 1999 Molecular cloning of FOG-2: A modulator of transcription factor GATA-4 in cardiomyocytes. Proc Natl Acad Sci USA 96:956-961
50. 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
51. Whitmarsh AJ, Davis RJ 2000 Regulation of transcription factor function by phosphorylation. Cell Mol Life Sci 57:1172-1183
52. Reinhart AJ, Williams SC, Clark BJ, Stocco DM 1999 SF-1 (steroidogenic factor-1) and C/EBPβ (CCAAT/enhancer binding protein-β) cooperate to regulate the murine StAR (steroidogenic acute regulatory) promoter. Mol Endocrinol 13:729-741
53. Yamaguchi Y, Nishio H, Kishi K, Ackerman SJ, Suda T 1999 C/EBPβ and GATA-1 synergistically regulate activity of the eosinophil granule major basic protein promoter: Implication for C/EBPβ activity in eosinophil gene expression. Blood 94:1429-1439
54. Wang X, Stocco DM 1999 Cyclic AMP and arachidonic acid: A tale of two pathways. Mol Cell Endocrinol 158:7-12
55. + in H295R adrenocortical cells. Mol Cell Endocrinol 115:215-219
56. Gyles SL, Burns CJ, Whitehouse BJ, Sugden D, Marsh PJ, Persaud SJ, Jones PM 2001 ERKs regulate cyclic AMP-induced steroid synthesis through transcription of the steroidogenic acute regulatory (STAR) gene. J Biol Chem 276: 34888-34895
57. Seger R, Hanoch T, Rosenberg R, Dantes A, Merz WE, Strauss III JF, Amsterdam A 2001 The ERK signaling cascade inhibits gonadotropin-stimulated steroidogenesis. J Biol Chem 276:13957-13964
58. Richards JS 2001 New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 15:209-218
59. Cooke BA 1990 Is cyclic AMP an obligatory second messenger for luteinizing hormone? Mol Cell Endocrinol 69:C11-C15
60. Daniel PB, Walker WH, Habener JF 1998 Cyclic AMP signaling and gene regulation. Annu Rev Nutr 18:353-383
61. 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
62. Liang Q, Wiese RJ, Bueno OF, Dai YS, Markham BE, Molkentin JD 2001 The transcription factor GATA-4 is activated by extracellular signal-regulated kinase 1- and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol Cell Biol 21:7460-7469
63. Yanazume T, Hasegawa K, Wada H, Morimoto T, Abe M, Kawamura T, Sasayama S 2002 Rho/ROCK pathway contributes to the activation of extracellular signal-regulated kinase/GATA-4 during myocardial cell hypertrophy. J Biol Chem 277:8618-8625
64. Charron F, Tsimiklis G, Arcand M, Robitaille L, Liang Q, Molkentin JD, Meloche S, Nemer M 2001 Tissue-specific GATA factors are transcriptional effectors of the small GTPase RhoA. Genes Dev 15:2702-2719
65. Hautala N, Tokola H, Luodonpaa M, Puhakka J, Romppanen H, Vuolteenaho O, Ruskoaho H 2001 Pressure overload increases GATA-4 binding activity via endothelin-1. Circulation 103:730-735
66. Kitta K, Clement SA, Remeika J, Blumberg JB, Suzuki YJ 2001 Endothelin-1 induces phosphorylation of GATA-4 transcription factor in the HL-1 atrial-muscle cell line. Biochem J 359:375-380
67. Morimoto T, Hasegawa K, Kaburagi S, Kakita T, Wada H, Yanazume T, Sasayama S 2000 Phosphorylation of GATA-4 is involved in α1-adrenergic agonist-responsive transcription of the endothelin-1 gene in cardiac myocytes. J Biol Chem 275:13721-13726
68. Kerkelä R, Pikkarainen S, Majalahti-Palviainen T, Tokola H, Ruskoaho H 2002 Distinct roles of mitogen activated protein kinase pathways in GATA-4 transcription factor mediated regulation of B-type natriuretic peptide gene. J Biol Chem 277:13752-13760
69. Partington GA, Patient RK 1999 Phosphorylation of GATA-1 increases its DNA-binding affinity and is correlated with induction of human K562 erythroleukaemia cells. Nucleic Acids Res 27:1168-1175
70. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE 1997 Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator: Coactivator interactions. Cell 91:741-752
71. Tremblay A, Tremblay GB, Labrie F, Giguere V 1999 Ligand-independent recruitment of SRC-1 to estrogen receptor β through phosphorylation of activation function AF-1. Mol Cell 3:513-519
72. Dai YS, Markham BE 2001 p300 Functions as a coactivator of transcription factor GATA-4. J Biol Chem 276:37178-37185
73. Querfurth E, Schuster M, Kulessa H, Crispino JD, Doderlein G, Orkin SH, Graf T, Nerlov C 2000 Antagonism between C/EBPβ and FOG in eosinophil lineage commitment of multipotent hematopoietic progenitors. Genes Dev 14:2515-2525