Maximal expression of FOXL2 in pituitary gonadotropes requires ovarian hormones

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Herndon, Maria K ^a   Nilson, John H ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; GONADORELIN; INHIBIN; INHIBIN BETA A; INHIBIN BETA B; LUTEINIZING HORMONE BETA SUBUNIT; MYELOPID; SMAD3 PROTEIN; THYROTROPIN BETA SUBUNIT; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN, MOUSE; SEX HORMONE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FOXL2 GENE; GENE; GENE EXPRESSION REGULATION; GONADORELIN RELEASE; GONADOTROPIN SECRETING CELL; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; IN VIVO STUDY; MOUSE; NONHUMAN; POLYSOME; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REPRODUCTIVE FITNESS; ANIMAL; ANTAGONISTS AND INHIBITORS; FEEDBACK SYSTEM; GENETICS; METABOLISM; OVARIECTOMY; OVARY;

ANIMALS; FEEDBACK, PHYSIOLOGICAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GONADAL HORMONES; GONADOTROPHS; GONADOTROPIN-RELEASING HORMONE; MICE; OVARIECTOMY; OVARY;

EID: 84957597161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126527     Document Type: Article

References (65)

1. Jorgensen JS, Quirk CC, Nilson JH. Multiple and overlapping combinatorial codes orchestrate hormonal responsiveness and dictate cell-specific expression of the genes encoding luteinizing hormone. Endocrine reviews. 2004;25(4):521-42. Epub 2004/08/06. doi: 10.1210/er.2003-0029 PMID: 15294880.
2. Thackray VG, Mellon PL, Coss D. Hormones in synergy: regulation of the pituitary gonadotropin genes. Molecular and cellular endocrinology. 2010;314(2):192-203. Epub 2009/09/15. doi: 10.1016/j.mce. 2009.09.003 PMID: 19747958; PubMed Central PMCID: PMC2815122.
3. Bilezikjian LM, Justice NJ, Blackler AN, Wiater E, Vale WW. Cell-type specific modulation of pituitary cells by activin, inhibin and follistatin. Molecular and cellular endocrinology. 2012;359(1-2):43-52. Epub 2012/02/15. doi: 10.1016/j.mce.2012.01.025 PMID: 22330643; PubMed Central PMCID: PMC3367026.
4. Hunzicker-Dunn M, Mayo KE. Gonadotropin Signaling in the Ovary, an Update. In: Neil JD, editor. The Physiology of Reproduction. 4 ed. San Diego, CA: Elsevier; 2014.
5. Ferris HA, Shupnik MA. Mechanisms for pulsatile regulation of the gonadotropin subunit genes by GNRH1. Biology of reproduction. 2006;74(6):993-8. Epub 2006/02/17. doi: 10.1095/biolreprod.105. 049049 PMID: 16481592.
6. Ciccone NA, Kaiser UB. The biology of gonadotroph regulation. Current opinion in endocrinology, diabetes, and obesity. 2009;16(4):321-7. Epub 2009/06/06. doi: 10.1097/MED.0b013e32832d88fb PMID: 19491666; PubMed Central PMCID: PMC2862266.
7. Dalkin AC, Haisenleder DJ, Ortolano GA, Ellis TR, Marshall JC. The frequency of gonadotropinreleasinghormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression. Endocrinology. 1989;125(2):917-24. Epub 1989/08/01. doi: 10.1210/endo-125-2-917 PMID: 2502379.
8. Bliss SP, Navratil AM, Xie J, Roberson MS. GnRH signaling, the gonadotrope and endocrine control of fertility. Frontiers in neuroendocrinology. 2010;31(3):322-40. Epub 2010/05/11. doi: 10.1016/j.yfrne. 2010.04.002 PMID: 20451543; PubMed Central PMCID: PMC2923852.
9. Corrigan AZ, Bilezikjian LM, Carroll RS, Bald LN, Schmelzer CH, Fendly BM, et al. Evidence for an autocrine role of activin B within rat anterior pituitary cultures. Endocrinology. 1991;128(3):1682-4. Epub 1991/03/01. PMID: 1900235.
10. Besecke LM, Guendner MJ, Sluss PA, Polak GG, Woodruff TK, Jameson JL, et al. Pituitary Follistatin Regulates Activin-Mediated Production of Follicle-Stimulating Hormone during the Rat Estrous Cycle. Endocrinology. 1997;138:2841-8. PMID: 9202226
11. Haisenleder DJ, Ortolano GA, Jolly D, Dalkin AC, Landefeld TD, Vale WW, et al. Inhibin secretion during the rat estrous cycle: relationships to FSH secretion and FSH beta subunit mRNA concentrations. Life sciences. 1990;47(19):1769-73. Epub 1990/01/01. PMID: 2123512.
12. Bilezikjian LM, Blount AL, Donaldson CJ, Vale WW. Pituitary actions of ligands of the TGF-beta family: activins and inhibins. Reproduction. 2006;132(2):207-15. Epub 2006/08/04. doi: 10.1530/rep. 1.01073 PMID: 16885530.
13. Bernard DJ, Lee KB, Santos MM. Activin B can signal through both ALK4 and ALK7 in gonadotrope cells. Reproductive biology and endocrinology: RB&E. 2006;4:52. Epub 2006/10/17. doi: 10.1186/1477-7827-4-52 PMID: 17040568; PubMed Central PMCID: PMC1617107.
14. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annual review of cell and developmental biology. 2005;21:659-93. doi: 10.1146/annurev. cellbio.21.022404.142018 PMID: 16212511.
15. Fortin J, Boehm U, Deng CX, Treier M, Bernard DJ. Follicle-stimulating hormone synthesis and fertility depend on SMAD4 and FOXL2. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2014;28(8):3396-410. doi: 10.1096/fj.14-249532 PMID: 24739304.
16. Suszko MI, Balkin DM, Chen Y, Woodruff TK. Smad3 mediates activin-induced transcription of folliclestimulating hormone beta-subunit gene. Molecular endocrinology (Baltimore, Md). 2005;19(7):1849-58. Epub 2005/03/12. doi: 10.1210/me.2004-0475 PMID: 15761025.
17. 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. Molecular endocrinology (Baltimore, Md). 2009;23(7):1001-13. Epub 2009/03/28. doi: 10.1210/me.2008-0324 PMID: 19324968; PubMed Central PMCID: PMC2703604.
18. 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. Molecular endocrinology (Baltimore, Md). 2010;24(5):1037-51. Epub 2010/03/18. doi: 10.1210/me.2009-0425 PMID: 20233786; PubMed Central PMCID: PMC2870942.
19. Tran S, Lamba P, Wang Y, Bernard DJ. SMADs and FOXL2 synergistically regulate murine FSHbeta transcription via a conserved proximal promoter element. Molecular endocrinology (Baltimore, Md). 2011;25(7):1170-83. Epub 2011/05/31. doi: 10.1210/me.2010-0480 PMID: 21622537.
20. Bernard DJ. Both SMAD2 and SMAD3 mediate activin-stimulated expression of the follicle-stimulating hormone beta subunit in mouse gonadotrope cells. Molecular endocrinology (Baltimore, Md). 2004;18(3):606-23. Epub 2004/01/01. doi: 10.1210/me.2003-0264 PMID: 14701940.
21. Lamba P, Santos MM, Philips DP, Bernard DJ. Acute regulation of murine follicle-stimulating hormone beta subunit transcription by activin A. Journal of molecular endocrinology. 2006;36(1):201-20. Epub 2006/02/08. doi: 10.1677/jme.1.01961 PMID: 16461939.
22. Roybal LL, Hambarchyan A, Meadows JD, Barakat NH, Pepa PA, Breen KM, et al. Roles of Binding Elements, FOXL2 Domains, and Interactions With cJUN and SMADs in Regulation of FSHbeta. Molecular endocrinology (Baltimore, Md). 2014;28(10):1640-55. Epub 2014/08/12. doi: 10.1210/me.2014-1008 PMID: 25105693; PubMed Central PMCID: PMC4179627.
23. Tran S, Zhou X, Lafleur C, Calderon MJ, Ellsworth BS, Kimmins S, et al. Impaired fertility and FSH synthesis in gonadotrope-specific Foxl2 knockout mice. Molecular endocrinology (Baltimore, Md). 2013;27(3):407-21. doi: 10.1210/me.2012-1286 PMID: 23340250; PubMed Central PMCID: PMC3589670.
24. Coss D, Mellon PL, Thackray VG. A FoxL in the Smad house: activin regulation of FSH. Trends in endocrinology and metabolism: TEM. 2010;21(9):562-8. Epub 2010/07/06. doi: 10.1016/j.tem.2010.05.006 PMID: 20598900; PubMed Central PMCID: PMC2933269.
25. Blount AL, Schmidt K, Justice NJ, Vale WW, Fischer WH, Bilezikjian LM. FoxL2 and Smad3 coordinately regulate follistatin gene transcription. The Journal of biological chemistry. 2009;284(12):7631-45. Epub 2008/12/25. doi: 10.1074/jbc. M806676200 PMID: 19106105; PubMed Central PMCID: PMC2658057.
26. Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, et al. Evolution and expression of FOXL2. Journal of medical genetics. 2002;39(12):916-21. PMID: 12471206; PubMed Central PMCID: PMC1757225.
27. 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. Molecular and cellular endocrinology. 2003;206(1-2):93-111. doi: 10.1016/s0303-7207 (03) 00235-1 PMID: 12943996
28. Liu Z, Wu F, Jiao B, Zhang X, Hu C, Huang B, et al. Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. The Journal of endocrinology. 2007;194(1):223-41. Epub 2007/06/27. doi: 10.1677/JOE-07-0135 PMID: 17592036.
29. Baron D, Cocquet J, Xia X, Fellous M, Guiguen Y, Veitia RA. An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. Journal of molecular endocrinology. 2004;33(3):705-15. Epub 2004/12/14. doi: 10.1677/jme.1.01566 PMID: 15591029.
30. Jiang W, Yang Y, Zhao D, Liu X, Duan J, Xie S, et al. Effects of sexual steroids on the expression of foxl2 in Gobiocypris rarus. Comparative biochemistry and physiology Part B, Biochemistry & molecular biology. 2011;160(4):187-93. Epub 2011/09/06. doi: 10.1016/j.cbpb.2011.08.005 PMID: 21889601.
31. Eozenou C, Vitorino Carvalho A, Forde N, Giraud-Delville C, Gall L, Lonergan P, et al. FOXL2 is regulated during the bovine estrous cycle and its expression in the endometrium is independent of conceptusderived interferon tau. Biology of reproduction. 2012;87(2):32. doi: 10.1095/biolreprod.112. 101584 PMID: 22623620.
32. Le Tissier PR, Hodson DJ, Lafont C, Fontanaud P, Schaeffer M, Mollard P. Anterior pituitary cell networks. Frontiers in neuroendocrinology. 2012;33(3):252-66. Epub 2012/09/18. doi: 10.1016/j.yfrne. 2012.08.002 PMID: 22981652.
33. Ibrahim SN, Moussa SM, Childs GV. Morphometric studies of rat anterior pituitary cells after gonadectomy: correlation of changes in gonadotropes with the serum levels of gonadotropins. Endocrinology. 1986;119(2):629-37. Epub 1986/08/01. PMID: 3089759.
34. Childs GV, Lloyd JM, Unabia G, Gharib SD, Wierman ME, Chin WW. Detection of luteinizing hormone beta messenger ribonucleic acid (RNA) in individual gonadotropes after castration: use of a new in situ hybridization method with a photobiotinylated complementary RNA probe. Molecular endocrinology (Baltimore, Md). 1987;1(12):926-32. Epub 1987/12/01. doi: 10.1210/mend-1-12-926 PMID: 3153470.
35. Charles MA, Mortensen AH, Potok MA, Camper SA. Pitx2 deletion in pituitary gonadotropes is compatible with gonadal development, puberty, and fertility. Genesis. 2008;46(10):507-14. Epub 2008/09/20. doi: 10.1002/dvg.20398 PMID: 18802953; PubMed Central PMCID: PMC2923441.
36. Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS. Cell-type-specific isolation of ribosomeassociated mRNA from complex tissues. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(33):13939-44. Epub 2009/08/12. 0907143106 [pii] doi: 10.1073/pnas. 0907143106 PMID: 19666516; PubMed Central PMCID: PMC2728999.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods (San Diego, Calif). 2001;25(4):402-8. Epub 2002/02/16. doi:10.1006/meth.2001.1262 PMID: 11846609.
38. Glidewell-Kenney C, Weiss J, Hurley LA, Levine JE, Jameson JL. Estrogen receptor alpha signaling pathways differentially regulate gonadotropin subunit gene expression and serum follicle-stimulating hormone in the female mouse. Endocrinology. 2008;149(8):4168-76. Epub 2008/05/10. doi: 10.1210/en. 2007-1807 PMID: 18467444; PubMed Central PMCID: PMC2488215.
39. Naik SI, Young LS, Saade G, Kujore A, Charlton HM, Clayton RN. Role of GnRH in the regulation of pituitary GnRH receptors in female mice. Journal of reproduction and fertility. 1985;74(2):605-14. Epub 1985/07/01. PMID: 2995657.
40. Couse JF, Yates MM, Walker VR, Korach KS. Characterization of the hypothalamic-pituitary-gonadal axis in estrogen receptor (ER) Null mice reveals hypergonadism and endocrine sex reversal in females lacking ERalpha but not ERbeta. Molecular endocrinology (Baltimore, Md). 2003;17(6):1039-53. doi: 10.1210/me.2002-0398 PMID: 12624116.
41. Keri RA, Wolfe MW, Saunders TL, Anderson I, Kendall SK, Wagner T, et al. The proximal promoter of the bovine luteinizing hormone beta-subunit gene confers gonadotrope-specific expression and regulation by gonadotropin-releasing hormone, testosterone, and 17 beta-estradiol in transgenic mice. Molecular endocrinology (Baltimore, Md). 1994;8(12):1807-16. Epub 1994/12/01. PMID: 7708066.
42. Fallest PC, Trader GL, Darrow JM, Shupnik MA. Regulation of rat luteinizing hormone beta gene expression in transgenic mice by steroids and a gonadotropin-releasing hormone antagonist. Biology of reproduction. 1995;53(1):103-9. Epub 1995/07/01. PMID: 7669840.
43. Saade G, London DR, Lalloz MR, Clayton RN. Regulation of LH subunit and prolactin mRNA by gonadal hormones in mice. Journal of molecular endocrinology. 1989;2(3):213-24. Epub 1989/05/01. PMID: 2751830.
44. Meinhardt UJ, Ho KK. Modulation of growth hormone action by sex steroids. Clinical endocrinology. 2006;65(4):413-22. doi: 10.1111/j.1365-2265.2006.02676.x PMID: 16984231.
45. Wen S, Schwarz JR, Niculescu D, Dinu C, Bauer CK, Hirdes W, et al. Functional characterization of genetically labeled gonadotropes. Endocrinology. 2008;149(6):2701-11. Epub 2008/03/08. doi: 10.1210/en. 2007-1502 PMID: 18325995.
46. Gore AJ, Philips DP, Miller WL, Bernard DJ. Differential regulation of follicle stimulating hormone by activin A and TGFB1 in murine gonadotropes. Reproductive biology and endocrinology: RB&E. 2005;3:73. Epub 2005/12/31. doi: 10.1186/1477-7827-3-73 PMID: 16384533; PubMed Central PMCID: PMC1351181.
47. Meunier H, Rivier C, Evans RM, Vale W. Gonadal and extragonadal expression of inhibin alpha, beta A, and beta B subunits in various tissues predicts diverse functions. Proceedings of the National Academy of Sciences of the United States of America. 1988;85(1):247-51. Epub 1988/01/01. PMID: 2829170; PubMed Central PMCID: PMC279521.
48. Bilezikjian LM, Corrigan AZ, Blount AL, Vale WW. Pituitary follistatin and inhibin subunit messenger ribonucleic acid levels are differentially regulated by local and hormonal factors. Endocrinology. 1996;137(10):4277-84. Epub 1996/10/01. doi: 10.1210/endo.137.10.8828487 PMID: 8828487.
49. Roberts V, Meunier H, Vaughan J, Rivier J, Rivier C, Vale W, et al. Production and regulation of inhibin subunits in pituitary gonadotropes. Endocrinology. 1989;124(1):552-4. Epub 1989/01/01. PMID: 2535814.
50. Coss D, Thackray VG, Deng CX, Mellon PL. Activin regulates luteinizing hormone beta-subunit gene expression through Smad-binding and homeobox elements. Molecular endocrinology (Baltimore, Md). 2005;19(10):2610-23. Epub 2005/06/18. doi: 10.1210/me.2005-0047 PMID: 15961509; PubMed Central PMCID: PMC2932483.
51. Wang Y, Fortin J, Lamba P, Bonomi M, Persani L, Roberson MS, et al. Activator protein-1 and smad proteins synergistically regulate human follicle-stimulating hormone beta-promoter activity. Endocrinology. 2008;149(11):5577-91. Epub 2008/07/26. doi: 10.1210/en. 2008-0220 PMID: 18653705; PubMed Central PMCID: PMC2584589.
52. Ellsworth BS, Egashira N, Haller JL, Butts DL, Cocquet J, Clay CM, et al. FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Molecular endocrinology (Baltimore, Md). 2006;20(11):2796-805. Epub 2006/07/15. doi: 10.1210/me.2005-0303 PMID: 16840539.
53. Ghochani Y, Saini JK, Mellon PL, Thackray VG. FOXL2 is involved in the synergy between activin and progestins on the follicle-stimulating hormone beta-subunit promoter. Endocrinology. 2012;153(4):2023-33. doi: 10.1210/en. 2011-1763 PMID: 22294749; PubMed Central PMCID: PMC3320250.
54. Elskus AA, Phelps AF, Schwartz NB. Acute sex differences in serum LH levels in gonadectomized rats: investigation of pituitary response to GnRH pulse frequency and prolactin secretion as etiological agents. Neuroendocrinology. 1995;61(3):301-9. PMID: 7898635.
55. Luderer U, Schwartz NB. Sex differences in acute luteinizing hormone responses to gonadectomy remain after progesterone antagonist and dopamine agonist treatment. Biology of reproduction. 1991;45(6):918-26. PMID: 1687201.
56. DePaolo LV. Hypersecretion of follicle-stimulating hormone (FSH) after ovariectomy of hypophysectomized, pituitary-grafted rats: implications for local regulatory control of FSH. Endocrinology. 1991;128(4):1731-40. Epub 1991/04/01. PMID: 1900775.
57. DePaolo LV, Bald LN, Fendly BM. Passive immunoneutralization with a monoclonal antibody reveals a role for endogenous activin-B in mediating FSH hypersecretion during estrus and following ovariectomy of hypophysectomized, pituitary-grafted rats. Endocrinology. 1992;130(3):1741-3. Epub 1992/03/01. PMID: 1537320.
58. Weiss J, Harris PE, Halvorson LM, Crowley WF Jr, Jameson JL. Dynamic regulation of follicle-stimulating hormone-beta messenger ribonucleic acid levels by activin and gonadotropin-releasing hormone in perifused rat pituitary cells. Endocrinology. 1992;131(3):1403-8. Epub 1992/09/11. PMID: 1505470.
59. Burger LL, Dalkin AC, Aylor KW, Workman LJ, Haisenleder DJ, Marshall JC. Regulation of gonadotropin subunit transcription after ovariectomy in the rat: measurement of subunit primary transcripts reveals differential roles of GnRH and inhibin. Endocrinology. 2001;142(8):3435-42. PMID: 11459788
60. Gharib SD, Wierman ME, Shupnik MA, Chin WW. Molecular biology of the pituitary gonadotropins. Endocrine reviews. 1990;11(1):177-99. Epub 1990/02/01. doi: 10.1210/edrv-11-1-177 PMID: 2108012.
61. Pannetier M, Renault L, Jolivet G, Cotinot C, Pailhoux E. Ovarian-specific expression of a new gene regulated by the goat PIS region and transcribed by a FOXL2 bidirectional promoter. Genomics. 2005;85(6):715-26. Epub 2005/05/12. doi: 10.1016/j.ygeno. 2005.02.011 PMID: 15885498.
62. Moumne L, Dipietromaria A, Batista F, Kocer A, Fellous M, Pailhoux E, et al. Differential aggregation and functional impairment induced by polyalanine expansions in FOXL2, a transcription factor involved in cranio-facial and ovarian development. Human molecular genetics. 2008;17(7):1010-9. Epub 2007/12/26. doi: 10.1093/hmg/ddm373 PMID: 18158309.
63. Benayoun BA, Georges AB, L'Hote D, Andersson N, Dipietromaria A, Todeschini AL, et al. Transcription factor FOXL2 protects granulosa cells from stress and delays cell cycle: role of its regulation by the SIRT1 deacetylase. Human molecular genetics. 2011;20(9):1673-86. Epub 2011/02/04. doi: 10.1093/hmg/ddr042 PMID: 21289058.
64. Clayton RN, Detta A, Naik SI, Young LS, Charlton HM. Gonadotrophin releasing hormone receptor regulation in relationship to gonadotrophin secretion. Journal of steroid biochemistry. 1985;23(5 B):691-702. Epub 1985/11/01. PMID: 3001413.
65. Naik SI, Young LS, Charlton HM, Clayton RN. Evidence for a pituitary site of gonadal steroid stimulation of GnRH receptors in female mice. Journal of reproduction and fertility. 1985;74(2):615-24. Epub 1985/07/01. PMID: 2995658.