Roles of binding elements, FOXL2 domains, And interactions with cJUN and SMADs in regulation of FSHβ

Molecular Endocrinology

Volumn 28, Issue 10, 2014, Pages 1640-1655

  Roybal, Lacey L ^a   Hambarchyan, Arpi ^a   Meadowa, Jason D ^a   Barakat, Nermeen H ^b   Pepa, Patricia A ^a   Breen, Kellie M ^a   Mellon, Pamela L ^a   Coss, Djurdjica ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; FOLLITROPIN; FOLLITROPIN BETA SUBUNIT; FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN; GONADORELIN; GONADOTROPIN; HYPOPHYSIS HORMONE; LUTEINIZING HORMONE; MUTANT PROTEIN; PROTEIN C JUN; SMAD PROTEIN; SMAD4 PROTEIN; UNCLASSIFIED DRUG; FOXL2 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LEVEL; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GONADOTROPIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; TRANSCRIPTION REGULATION; WILD TYPE; ANIMAL; GENETIC TRANSCRIPTION; GENETICS; GONADOTROPIN SECRETING CELL; HYPOPHYSIS; KNOCKOUT MOUSE; METABOLISM; ONCOGENE; PHYSIOLOGY;

ANIMALS; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENES, JUN; GONADOTROPHS; MICE; MICE, KNOCKOUT; PITUITARY GLAND; PROMOTER REGIONS, GENETIC; SMAD PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84907623282     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1008     Document Type: Article

References (47)

1. Woodruff TK, Besecke LM, Groome N, Draper LB, Schwartz NB, Weiss J. Inhibin A and inhibin B are inversely correlated to folliclestimulating hormone, yet are discordant during the follicular phase of the rat estrous cycle, and inhibin A is expressed in a sexually dimorphic manner. Endocrinology. 1996;137:5463–5467.
2. Besecke LM, Guendner MJ, Sluss PA, et al. Pituitary follistatin regulates activin-mediated production of follicle-stimulating hormone during the rat estrous cycle. Endocrinology. 1997;138:2841–2848.
3. Chand AL, Harrison CA, Shelling AN. Inhibin and premature ovarian failure. Hum Reprod Update. 2010;16:39–50.
4. Kaiser UB, Conn PM, Chin WW. Studies of gonadotropin-releasing hormone (GnRH) action using GnRH receptor-expressing pituitary cell lines. Endocr Rev. 1997;18:46–70.
5. Vale W, Rivier C, Brown M. Regulatory peptides of the hypothalamus. Annu Rev Physiol. 1977;39:473–527.
6. Weiss J, Guendner MJ, Halvorson LM, Jameson JL. Transcriptional activation of the follicle-stimulating hormone beta-subunit gene by activin. Endocrinology. 1995;136:1885–1891.
7. Coss D, Hand CM, Yaphockun KK, Ely HA, Mellon PL. p38 mitogen- activated protein kinase is critical for synergistic induction of the FSH(beta) gene by gonadotropin-releasing hormone and activin through augmentation of c-Fos induction and Smad phosphorylation. Mol Endocrinol. 2007;21:3071–3086.
8. Ling N, Ying SY, Ueno N, et al. Pituitary FSH is released by a heterodimer of the beta-subunits from the two forms of inhibin. Nature. 1986;321:779–782.
9. Gregory SJ, Lacza CT, Detz AA, Xu S, Petrillo LA, Kaiser UB. Synergy between activin A and gonadotropin-releasing hormone in transcriptional activation of the rat follicle-stimulating hormonebeta gene. Mol Endocrinol. 2005;19:237–254.
10. Suszko MI, Balkin DM, Chen Y, Woodruff TK. Smad3 mediates activin-induced transcription of follicle-stimulating hormone betasubunit gene. Mol Endocrinol. 2005;19:1849–1858.
11. Bernard DJ. Both SMAD2 and SMAD3 mediate activin-stimulated expression of the follicle-stimulating hormone beta subunit in mouse gonadotrope cells. Mol Endocrinol. 2004;18:606–623.
12. McGillivray SM, Thackray VG, Coss D, Mellon PL. Activin and glucocorticoids synergistically activate follicle-stimulating hormone beta-subunit gene expression in the immortalized LbetaT2 gonadotrope cell line. Endocrinology. 2007;148:762–773.
13. Lamba P, Fortin J, Tran S, Wang Y, Bernard DJ. A novel role for the forkhead transcription factor FOXL2 in activin A-regulated follicle- stimulating hormone beta subunit transcription. Mol Endocrinol. 2009;23:1001–1013.
14. Lamba P, Wang Y, Tran S, et al. Activin A regulates porcine folliclestimulating hormone beta-subunit transcription via cooperative actions of SMADs and FOXL2. Endocrinology. 2010;151:5456–5467.
15. Corpuz PS, Lindaman LL, Mellon PL, Coss D. FoxL2 is required for activin induction of the mouse and human follicle-stimulating hormone beta-subunit genes. Mol Endocrinol. 2010;24:1037–1051.
16. Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol. 2002;250:1–23.
17. Ellsworth BS, Egashira N, Haller JL, et al. FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol Endocrinol. 2006;20:2796–2805.
18. Blount AL, Schmidt K, Justice NJ, Vale WW, Fischer WH, Bilezikjian LM. FoxL2 and Smad3 coordinately regulate follistatin gene transcription. J Biol Chem. 2009;284:7631–7645.
19. Wang Y, Libasci V, Bernard DJ. Activin A induction of FSHbeta subunit transcription requires SMAD4 in immortalized gonadotropes. J Mol Endocrinol. 2010;44:349–362.
20. Tran S, Lamba P, Wang Y, Bernard DJ. SMADs and FOXL2 synergistically regulate murine FSHbeta transcription via a conserved proximal promoter element. Mol Endocrinol. 2011;25:1170–1183.
21. Ellsworth BS, Burns AT, Escudero 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.
22. Kuo FT, Fan K, Bentsi-Barnes I, Barlow GM, Pisarska MD. Mouse forkhead L2 maintains repression of FSH-dependent genes in the granulosa cell. Reproduction. 2012;144:485–494.
23. Pisarska MD, Barlow G, Kuo FT. Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology. 2011;152:1199–1208.
24. McTavish KJ, Nonis D, Hoang YD, Shimasaki S. Granulosa cell tumor mutant FOXL2C134W suppresses GDF-9 and activin A-induced follistatin transcription in primary granulosa cells. Mol Cell Endocrinol. 2013;372:57–64.
25. Pisarska MD, Kuo FT, Bentsi-Barnes IK, Khan S, Barlow GM. LATS1 phosphorylates forkhead L2 and regulates its transcriptional activity. Am J Physiol Endocrinol Metab. 2010;299:E101–E109.
26. Crisponi L, Deiana M, Loi A, et al. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat Genet. 2001;27:159–166.
27. De Baere E, Beysen D, Oley C, et al. FOXL2 and BPES: mutational hotspots, phenotypic variability, and revision of the genotype-phenotype correlation. Am J Hum Genet. 2003;72:478–487.
28. Uda M, Ottolenghi C, Crisponi L, et al. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet. 2004;13:1171–1181.
29. Schmidt D, Ovitt CE, Anlag K, et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development. 2004;131:933–942.
30. Justice NJ, Blount AL, Pelosi E, Schlessinger D, Vale W, Bilezikjian LM. Impaired FSHbeta expression in the pituitaries of Foxl2 mutant animals. Mol Endocrinol. 2011;25:1404–1415.
31. Tran S, Zhou X, Lafleur C, et al. Impaired fertility and FSH synthesis in gonadotrope-specific Foxl2 knockout mice. Mol Endocrinol. 2013;27:407–421.
32. Coss D, Jacobs SB, Bender CE, Mellon PL. A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone beta gene by gonadotropin-releasing hormone. J Biol Chem. 2004; 279:152–162.
33. Mollard P, Hodson DJ, Lafont C, Rizzoti K, Drouin J. A tridimensional view of pituitary development and function. Trends Endocrinol Metab. 2012;23:261–269.
34. Park M, Shin E, Won M, et al. FOXL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1-induced CYP17 transcription in granulosa cells. Mol Endocrinol. 2010;24:1024–1036.
35. Bailey JS, Rave-Harel N, McGillivray SM, Coss D, Mellon PL. Activin regulation of the follicle-stimulating hormone beta-subunit gene involves Smads and the TALE homeodomain proteins Pbx1 and Prep1. Mol Endocrinol. 2004;18:1158–1170.
36. Ghochani Y, Saini JK, Mellon PL, Thackray VG. FOXL2 is involved in the synergy between activin and progestins on the folliclestimulating hormone β-subunit promoter. Endocrinology. 2012; 153:2023–2033.
37. Coss D, Mellon PL, Thackray VG. A FoxL in the Smad house: activin regulation of FSH. Trends Endocrinol Metab. 2010;21: 562–568.
38. Qing J, Zhang Y, Derynck R. Structural and functional characterization of the transforming growth factor-beta -induced Smad3/c- Jun transcriptional cooperativity. J Biol Chem. 2000;275:38802–38812.
39. Coss D, Thackray VG, Deng CX, Mellon PL. Activin regulates luteinizing hormone beta-subunit gene expression through smadbinding and homeobox elements. Mol Endocrinol. 2005;19:2610–2623.
40. Stouffer RL, Woodruff TK, Dahl KD, Hess DL, Mather JP, Molskness TA. Human recombinant activin-A alters pituitary luteinizing hormone and follicle-stimulating hormone secretion, follicular development, and steroidogenesis, during the menstrual cycle in rhesus monkeys. J Clin Endocrinol Metab. 1993;77:241–248.
41. Blumenfeld Z, Ritter M. Inhibin, activin, and follistatin in human fetal pituitary and gonadal physiology. Ann NY Acad Sci. 2001; 943:34–48.
42. Caburet S, Georges A, L’Hôte D, Todeschini AL, Benayoun BA, Veitia RA. The transcription factor FOXL2: at the crossroads of ovarian physiology and pathology. Mol Cell Endocrinol. 2012;356: 55–64.
43. 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.
44. De Baere E, Dixon MJ, Small KW, et al. Spectrum of FOXL2 gene mutations in blepharophimosis-ptosis-epicanthus inversus (BPES) families demonstrates a genotype–phenotype correlation. Hum Mol Genet. 2001;10:1591–1600.
45. Benson CA, Kurz TL, Thackray VG. Ahuman FSHB promoter SNP associated with low FSH levels in men impairs LHX3 binding and basal FSHB transcription. Endocrinology. 2013;154:3016–3021.
46. West BE, Parker GE, Savage JJ, et al. Regulation of the folliclestimulating hormone beta gene by the LHX3 LIM-homeodomain transcription factor. Endocrinology. 2004;145:4866–4879.
47. Thackray VG, Mellon PL, Coss D. Hormones in synergy: regulation of the pituitary gonadotropin genes. Mol Cell Endocrinol. 2010;314:192–203.