Synergistic activation of the Mc2r promoter by FOXL2 and NR5A1 in mice

Biology of Reproduction

Volumn 83, Issue 5, 2010, Pages 842-851

  Yang, Wei Hsiung ^a   Gutierrez, Ninoska M ^a   Wang, Lizhong ^b   Ellsworth, Buffy S ^c   Wang, Chiung Min ^a  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adrenal; Adrenal cortex; FOXL2; Gene regulation; Mc2r; NR5A1; Ovary; Star; Steroid hormone receptors; Transcription regulation

Indexed keywords

BETA ACTIN; BIOCHEMICAL MARKER; CHOLESTEROL; FORKHEAD TRANSCRIPTION FACTOR; MELANOCORTIN 2 RECEPTOR; PROTEIN FOXL2; STEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROIDOGENIC FACTOR 1; UNCLASSIFIED DRUG;

ADRENAL GLAND; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLEPHAROPHIMOSIS PTOSIS EPICANTHUS INVERSUS SYNDROME; CHOLESTEROL METABOLISM; CONTROLLED STUDY; CYP19A1A GENE; DNA RESPONSIVE ELEMENT; FEMALE; FISH; FOXL2 GENE; GENE; GENE ACTIVATION; GENE MAPPING; GENE MUTATION; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; MAMMAL; MC2R GENE; METABOLIC REGULATION; MOUSE; NONHUMAN; OVARY DEVELOPMENT; OVARY FUNCTION; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STAR GENE; STEROID METABOLISM; STEROIDOGENESIS; SYNDROME; TRANSCRIPTION REGULATION; UPREGULATION;

ADRENAL GLANDS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; MALE; MICE; ORGAN SPECIFICITY; OVARY; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; RECEPTOR, MELANOCORTIN, TYPE 2; RESPONSE ELEMENTS; RNA, MESSENGER; STEROIDOGENIC FACTOR 1;

MAMMALIA; MUS;

EID: 77958610270     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.085621     Document Type: Article

References (46)

1. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994; 77:481-490.
2. Hammer GD, Ingraham HA. Steroidogenic factor-1: its role in endocrine organ development and differentiation. Front Neuroendocrinol 1999; 20:199-223.
3. Val P, Lefrancois-Martinez AM, Veyssiere G, Martinez A. SF-1 a key player in the development and differentiation of steroidogenic tissues. Nucl Recept 2003; 1:8.
4. Carlone DL, Richards JR. 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 1997; 11:292-304.
5. Sugawara T, Holt JA, Kiriakidou M, Strauss JF III. Steroidogenic factor 1-dependent promoter activity of the human steroidogenic acute regulatory protein (StAR) gene. Biochemistry 1996; 35:9052-9059.
6. Winnay JN, Hammer GD. Adrenocorticotropic hormone-mediated signaling cascades coordinate a cyclic pattern of steroidogenic factor 1-dependent transcriptional activation. Mol Endocrinol 2006; 20:147-166.
7. Dorn C, Ou Q, Svaren J, Crawford PA, Sadovsky Y. Activation of luteinizing hormone b gene by gonadotropin-releasing hormone requires the synergy of early growth response-1 and steroidogenic factor-1. J Biol Chem 1999; 274:13870-13876.
8. Tremblay JJ, Viger RS. Transcription factor GATA-4 enhances Mullerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol Endocrinol 1999; 13:1388-1401.
9. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 1998; 18:6653-6665.
10. Hossain A, Saunders GF. Role of Wilms tumor 1 (WT1) in the transcriptional regulation of the Mullerian-inhibiting substance promoter. Biol Reprod 2003; 69:1808-1814.
11. Ito M, Yu RN, Jameson JL. Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol Endocrinol 1998; 12:290-301.
12. Chen WY, Juan LJ, Chung BC. SF-1 (nuclear receptor 5A1) activity is activated by cyclic AMP via p300-mediated recruitment to active foci, acetylation, and increased DNA binding. Mol Cell Biol 2005; 25:10442-10453.
13. Borud B, Hoang T, Bakke M, Jacob AL, Lund J, Mellgren G. 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 2002; 16:757-773.
14. Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, Weigel NL, Ingraham HA. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol Cell 1999; 3:521-526.
15. Mizusaki H, Kawabe K, Mukai T, Ariyoshi E, Kasahara M, Yoshioka H, Swain A, Morohashi K. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenital critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol Endocrinol 2003; 17:507-519.
16. Crawford PA, Dorn C, Sadovsky Y, Millbrandt J. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 1998; 18:2949-2956.
17. Ito M, Yu RN, Jameson JL. DAX-1 inhibits SF-1-mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenital. Mol Cell Biol 1997; 17:1476-1483.
18. Ou Q, Mouillet JF, Yan X, Dorn C, Crawford PA, Sadovsky Y. The DEAD box protein DP103 is a regulator of steroidogenic factor-1. Mol Endocrinol 2001; 15:69-79.
19. Campbell LA, Faivre EJ, Show MD, Ingraham JG, Flinders J, Gross JD, Ingraham HA. Decreased recognition of SUMO-sensitive target genes following modification of SF-1 (NR5A1). Mol Cell Biol 2008; 28:7476-7486.
20. Yang WH, Heaton JH, Brevig H, Mukherjee S, Iniguez-Lluhi JA, Hammer GD. SUMOylation inhibits SF-1 activity by reducing CDK7-mediated serine 203 phosphorylation. Mol Cell Biol 2009; 29:613-625.
21. Krylova IN, Sablin EP, Moore RX, Xu RX, Waitt GM, Mackay JA, Juzumiene D, Bynum JM, Madauss K, Montana V, Lebedeva L, Suzawa M, Williams JD, Williams SP, Guy RK, Thornton JW, Fletterick RJ, Wilson TM, Ingraham HA. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell 2005; 120:343-355.
22. Li Y, Choi M, Cavey G, Daughterty J, Suino K, Kovach A, Bingham NC, Kliewer SA, Xu HE. Crystallographic identification and functional characterization of phospholipids as ligands for the orphan nuclear receptor steroidogenic factor-1. Mol Cell 2005; 17:491-502.
23. Else T, Hammer GD. Genetic analysis of adrenal absence: agenesis and aplasia. Trends Endocrinol Metab 2005; 16:458-468.
24. Coutant R, Mallet D, Lahlou N, Bouhours-Nouet N, Guichet A, Coupris L, Croue A, Morel Y. Heterozygous mutation of steroidogenic factor-1 in 46, XY subjects may mimic partial androgen insensitivity syndrome. J Clin Endocrinol Metab 2007; 92:2868-2873.
25. Lourenco D, Brauner R, Lin L, De Perdigo A, Weryha G, Muresan M, Boudjenah R, Guerra-Junior G, Maciel-Guerra AT, Achermann JC, McElreavey K, Bashamboo A. Mutations in NR5A1 associated with ovarian insufficiency. N Engl J Med 2009; 360:1200-1210.
26. Moumne L, Batista F, Benayoun BA, Nallathambi J, Fellous M, Sundaresan P, Veitia RA. The mutations and potential targets of the forkhead transcription factor FOXL2. Mol Cell Endocrinol 2008; 282:2-11.
27. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, De Baere E, Messiaen L, Cotinot C, Fellous M, Veitia RA. Evolution and expression of FOXL2. J Med Genet 2002; 39:916-921.
28. Cocquet J, De Baere E, Gareil M, Pannetier M, Xia X, Fellous M, Veitia RA. Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet Genome Res 2003; 101:206-211.
29. Ellsworth BS, Egashira N, Haller JL, Butts DL, Cocquet J, Clay CM, Osamura RY, Camper SA. Foxl2 in the pituitary: molecular, genetic, and developmental analysis. Mol Endocrinol 2006; 20:2796-2805.
30. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 2004; 131:933-942.
31. Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, Kimber W, Forabosco A, Cao A, Schlessinger D, Pilia J. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 2004; 13:1171-1181.
32. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier AC, Klugmann C, Klasen C, Holter NI, Riethmacher D, Schutz G, Cooney AJ, Lovell-Badge R, Treier M. Somatic sex programming of adult ovaries to testes by Foxl2 ablation. Cell 2009; 139:1130-1142.
33. Ellsworth BS, Burn AT, Escodero KW, Duval DL, Nelson SE, Clay CM. The gonadotropin releasing hormone (GnRH) receptor activating sequence (GRAS) is a composite regulatory element that interacts with multiple classes of transcription factors including Smads, AP-1 and a forkhead DNA binding protein. Mol Cell Endocrinol 2003; 206:93-111.
34. Batista F, Vaiman D, Dausset J, Fellous M, Veitia RA. Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. Proc Natl Acad Sci U S A 2007; 104:3330-3335.
35. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pépin B, Cotinot C, Veitia R, Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 2006; 36:399-413.
36. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 2007; 21:712-725.
37. Pisarska MD, Bae J, Klein C, Hsueh AJ. Forkhead L2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 2004; 145:3424-3433.
38. Bentsi-Barnes IK, Kuo FT, Barlow GM, Pisarska MD. Human forkhead L2 represses key genes in granulosa cell differentiation including aromatase, P450scc, and cyclin D2. Fertil Steril 2010; 94:353-356.
39. Kalfa N, Fellous M, Boizet-Bonhoure B, Patte C, Duvillard P, Pienkowski C, Jaubert F, Ecochard A, Sultan C. Aberrant expression of ovary determining gene Foxl2 in the testis and juvenile granulosa cell tumor in children. J Urol 2008; 180:1810-1813.
40. Benayoun BA, Kalfa N, Sultan C, Veitia RA. The forkhead factor Foxl2: a novel tumor suppressor? Biochim Biophys Acta 2009; 1805:1-5.
41. Kobel M, Gilks CB, Huntsman DG. Adult-type granulosa cell tumors and Foxl2 mutation. Cancer Res 2009; 69:9160-9162.
42. Lewis AE, Rusten M, Hoivik EA, Vikse EL, Hansson ML, Wallberg AE, Bakke M. Phosphorylation of steroidogenic factor 1 is mediated by cyclin-dependent kinase 7. Mol Endocrinol 2008; 22:91-104.
43. Park M, Shin E, Won M, Kim JH, Go H, Kim HL, Ko JJ, Lee K, Bae J. FoxL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1- induced CYP17 transcription in granulosa cells. Mol Endocrinol 2010; 24:1024-1036.
44. Frigeri C, Tsao J, Czerwinski W, Schimmer BP. Impaired steroidogenic factor 1 (NR5A1) activity in mutant Y1 mouse adrenocortical tumor cells. Mol Endocrinol 2000; 14:535-544.
45. Kuo FT, Bentsi-Barnes IK, Barlow GM, Bae J, Pisarska MD. Sumoylation of forkhead L2 by Ubc9 is required for its activity as a transcriptional repressor of the steroidogenic acute regulatory gene. Cell Signal 2009; 21:1935-1944.
46. Marongiu M, Deiana M, Meloni A, Marcia L, Puddu A, Cao A, Schlessinger D, Crisponi L. The forkhead transcription factor Foxl2 is sumoylated in both human and mouse: sumoylation affects its stability, localization, and activity. PLos One 2010; 5:e9477.