FOXL2: A central transcription factor of the ovary

Journal of Molecular Endocrinology

Volumn 52, Issue 1, 2013, Pages

  Georges, Adrien ^a,b   Auguste, Aurelie ^a,b   Bessière, Laurianne ^a,b   Vanet, Anne ^a,b   Todeschini, Anne Laure ^a,b   Veitia, Reiner A ^a,b  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cancer; FOXL2; Oestrogen receptors; Ovarian function; Ovary

Indexed keywords

ESTROGEN; FORKHEAD TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; ESTROGEN SYNTHESIS; GENE EXPRESSION REGULATION; GENE REPRESSION; GRANULOSA CELL; GRANULOSA CELL TUMOR; HUMAN; NONHUMAN; OVARY; OVARY CANCER; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; OVULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; REVIEW; SEX DETERMINATION; SOMATIC MUTATION; TRANSCRIPTION REGULATION;

CANCER; FOXL2; OESTROGEN RECEPTORS; OVARIAN FUNCTION; OVARY;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GRANULOSA CELLS; HUMANS; OVARIAN FOLLICLE; OVARY; SEX DETERMINATION PROCESSES;

EID: 84890878682     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-13-0159     Document Type: Review

References (126)

1. Adhikari D. & Liu K 2009 Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocrine Reviews 30 438-464. (doi:10.1210/er.2008-0048)
2. Andreu-Vieyra C., Chen R & Matzuk MM 2008 Conditional deletion of the retinoblastoma (Rb) gene in ovarian granulosa cells leads to premature ovarian failure. Molecular Endocrinology 22 2141-2161. (doi:10.1210/ me.2008-0033)
3. Auguste A., Chassot A-A, Grégoire EP, Renault L, Pannetier M, Treier M, Pailhoux E. & Chaboissier M-C 2011 Loss of R-spondin1 and Foxl2 amplifies female-to-male sex reversal in XX mice. Sexual Development 5 304-317. (doi:10.1159/000334517)
4. Baarends WM, Uilenbroek JT, Kramer P, Hoogerbrugge JW, van Leeuwen EC, Themmen A. P & Grootegoed JA 1995 Anti-Müllerian hormone and anti-Müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 136 4951-4962. (doi:10.1210/en.136.11.4951)
5. Barrionuevo F., Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C & Scherer G. 2006 Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biology of Reproduction 74 195-201. (doi:10.1095/ biolreprod.105.045930)
6. Batista F., Vaiman D, Dausset J, FellousM& Veitia RA 2007 Potential targets of FOXL2, a transcription factor involved in craniofacial and follicular development, identified by transcriptomics. PNAS 104 3330-3335. (doi:10.1073/pnas.0611326104)
7. Beamer W. G, Hoppe PC & Whitten WK 1985 Spontaneous malignant granulosa cell tumors in ovaries of young SWRmice. Cancer Research 45 5575-5581.
8. Benayoun B. A, Batista F, Auer J, Dipietromaria A, L'Hôte D, De Baere E & Veitia R. A 2009 Positive and negative feedback regulates the transcription factor FOXL2 in response to cell stress: evidence for a regulatory imbalance induced by disease-causing mutations. Human Molecular Genetics 18 632-644. (doi:10.1093/hmg/ddn389)
9. Benayoun B. A, Caburet S, Dipietromaria A, Georges A, D'Haene B, Pandaranayaka P. JE, L'Hôte D, Todeschini A-L, Krishnaswamy S, FellousM et al. 2010 Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p. Cys134Trp (c.402COG). PLoS ONE 5 e8789. (doi:10.1371/journal.pone.0008789)
10. Benayoun B. A, Anttonen M, L'Hôte D, Bailly-Bechet M, Andersson N, Heikinheimo M. & Veitia RA 2013 Adult ovarian granulosa cell tumor transcriptomics: prevalence of FOXL2 target genes misregulation gives insights into the pathogenic mechanism of the p. Cys134Trp somatic mutation. Oncogene 32 2739-2746. (doi:10.1038/onc.2012.298)
11. Bentsi-Barnes I. K, Kuo F-T, Barlow GM & Pisarska MD 2010 Human forkhead L2 represses key genes in granulosa cell differentiation including aromatase, P450scc, and cyclin D2. Fertility and Sterility 94 353-356. (doi:10.1016/j.fertnstert.2009.09.050)
12. Bernard P., Sim H, Knower K, Vilain E & Harley V 2008 Human SRY inhibits b-catenin-mediated transcription. International Journal of Biochemistry & Cell Biology 40 2889-2900. (doi:10.1016/j.biocel.2008.06.006)
13. Blount A. L, Schmidt K, Justice NJ, Vale WW, Fischer WH & Bilezikjian LM 2009 FoxL2 and Smad3 coordinately regulate follistatin gene transcription. Journal of Biological Chemistry 284 7631-7645. (doi:10.1074/jbc.M806676200)
14. Boerboom D., Paquet M, Hsieh M, Liu J, Jamin SP, Behringer RR, Sirois J, Taketo M. M & Richards JS 2005 Misregulated Wnt/b-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Research 65 9206-9215. (doi:10.1158/0008-5472.CAN-05-1024)
15. Boulanger L., Kocer A, Daniel N, Pannetier M, Chesné P, Heyman Y, Renault L, Mandon-Pépin B, Chavatte-Palmer P, Vignon X et al. 2008 Attempt to rescue sex-reversal by transgenic expression of the PISRT1 gene in XX PISK/K goats. Sexual Development 2 142-151. (doi:10.1159/000143432)
16. Burns K. H, Agno JE, Chen L, Haupt B, Ogbonna SC, Korach KS & Matzuk M. M 2003 Sexually dimorphic roles of steroid hormone receptor signaling in gonadal tumorigenesis. Molecular Endocrinology 17 2039-2052. (doi:10.1210/me.2003-0039)
17. Caburet S., Georges A, L'Hôte D, Todeschini A-L, Benayoun BA & Veitia RA 2012 The transcription factor FOXL2: at the crossroads of ovarian physiology and pathology. Molecular and Cellular Endocrinology 356 55-64. (doi:10.1016/j.mce.2011.06.019)
18. Carlsson I. B, Scott JE, Visser JA, Ritvos O, Themmen APN & Hovatta O 2006 Anti-Müllerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Human Reproduction 21 2223-2227. (doi:10.1093/humrep/del165)
19. Chaboissier M.-C, Kobayashi A, Vidal VIP, Lützkendorf S, van de Kant HJG, Wegner M., de Rooij DG, Behringer RR & Schedl A 2004 Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131 1891-1901. (doi:10.1242/dev.01087)
20. Chassot A.-A, Ranc F, Gregoire EP, Roepers-Gajadien HL, Taketo MM, Camerino G., de Rooij DG, Schedl A & Chaboissier M-C 2008 Activation of b-catenin signaling by Rspo1 controls differentiation of the mammalian ovary. Human Molecular Genetics 17 1264-1277. (doi:10.1093/hmg/ddn016)
21. Cheng J.-C, Klausen C & Leung PCK 2013 Overexpression of wild-type but not C134W mutant FOXL2 enhances Gn RH-induced cell apoptosis by increasing Gn RH receptor expression in human granulosa cell tumors. PLoS ONE 8 e55099. (doi:10.1371/journal.pone.0055099)
22. Choi Y., Ballow DJ, Xin Y & Rajkovic A 2008a Lim homeobox gene, Lhx8, is essential for mouse oocyte differentiation and survival. Biology of Reproduction 79 442-449. (doi:10.1095/biolreprod.108.069393)
23. Choi Y., Yuan D & Rajkovic A 2008b Germ cell-specific transcriptional regulator Sohlh2 is essential for early mouse folliculogenesis and oocytespecific gene expression. Biology of Reproduction 79 1176-1182. (doi:10.1095/biolreprod.108.071217)
24. Cocquet J., Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M, Baere ED, Messiaen L., Cotinot C, Fellous M et al. 2002 Evolution and expression of FOXL2. Journal of Medical Genetics 39 916-921. (doi:10.1136/jmg.39. 12.916)
25. Cocquet J., Baere ED, Gareil M, Pannetier M, Xia X, Fellous M & Veitia RA 2003 Structure, evolution and expression of the FOXL2 transcription unit. Cytogenetic and Genome Research 101 206-211. (doi:10.1159/ 000074338)
26. Combes A. N, Spiller CM, Harley VR, Sinclair AH, Dunwoodie SL, Wilhelm D & Koopman P 2010 Gonadal defects in Cited2-mutant mice indicate a role for SF1 in both testis and ovary differentiation. International Journal of Developmental Biology 54 683-689. (doi:10.1387/ijdb. 092920ac)
27. Corpuz P. S, Lindaman LL, Mellon PL & Coss D 2010 FoxL2 is required for activin induction of the mouse and human follicle-stimulating hormone b-subunit genes. Molecular Endocrinology 24 1037-1051. (doi:10.1210/me.2009-0425)
28. Crisponi L., Deiana M, Loi A, Chiappe F, Uda M, Amati P, Bisceglia L, Zelante L., Nagaraja R, Porcu S et al. 2001 The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/ epicanthus inversus syndrome. Nature Genetics 27 159-166. (doi:10.1038/84781)
29. Dai A., Sun H, Fang T, Zhang Q, Wu S, Jiang Y, Ding L, Yan G & Hu Y 2013 Micro RNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2. FEBS Letters 587 2474-2482. (doi:10.1016/j.febslet.2013.06.023)
30. Danesin C. & Houart C 2012 A Fox stops the Wnt: implications for forebrain development and diseases. Current Opinion in Genetics & Development 22 323-330. (doi:10.1016/j.gde.2012.05.001)
31. De Santa Barbara P., Méjean C, Moniot B, Malcle's MH, Berta P & Boizet-Bonhoure B. 2001 Steroidogenic factor-1 contributes to the cyclic-adenosine monophosphate down-regulation of human SRY gene expression. Biology of Reproduction 64 775-783. (doi:10.1095/biolreprod64.3.775)
32. De Vos M., Devroey P & Fauser BC 2011 Primary ovarian insufficiency. Lancet 376 911-921. (doi:10.1016/S0140-6736(10)60355-8)
33. Dipietromaria A., Benayoun BA, Todeschini A-L, Rivals I, BazinC&Veitia RA 2009 Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems. Human Molecular Genetics 18 3324-3333. (doi:10.1093/hmg/ddp273)
34. Dupont S., Krust A, Gansmuller A, Dierich A, Chambon P & Mark M 2000 Effect of single and compound knockouts of estrogen receptors a (ERa) and b (ERb) on mouse reproductive phenotypes. Development 127 4277-4291.
35. Durlinger A. LL, Kramer P, Karels B, de Jong FH, Uilenbroek JTJ, Grootegoed J. A & Themmen APN 1999 Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 140 5789-5796. (doi:10.1210/en.140.12.5789)
36. Edson M. A, Nagaraja AK & Matzuk MM 2009 The mammalian ovary from genesis to revelation. Endocrine Reviews 30 624-712. (doi:10.1210/ er.2009-0012)
37. Edson M. A, Nalam RL, Clementi C, Franco HL, Demayo FJ, Lyons KM, Pangas S. A & Matzuk MM 2010 Granulosa cell-expressed BMPR1A and BMPR1B have unique functions in regulating fertility but act redundantly to suppress ovarian tumor development. Molecular Endocrinology 24 1251-1266. (doi:10.1210/me. 2009-0461)
38. El-Dahr S. S, Aboudehen K & Saifudeen Z 2008 Transcriptional control of terminal nephron differentiation. American Journal of Physiology. Renal Physiology 294 F1273-F1278. (doi:10.1152/ajprenal.00562.2007)
39. Ellsworth B. S, Burns AT, Escudero KW, Duval DL, Nelson SE & Clay CM 2003 The gonadotropin releasing hormone (Gn RH) 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 206 93-111. (doi:10.1016/S0303-7207(03)00235-1)
40. Escudero J. M, Haller JL, Clay CM & Escudero KW 2010 Microarray analysis of Foxl2 mediated gene regulation in the mouse ovary derived KK1 granulosa cell line: over-expression of Foxl2 leads to activation of the gonadotropin releasing hormone receptor gene promoter. Journal of Ovarian Research 3 4. (doi:10.1186/1757-2215-3-4)
41. Fisher C. R, Graves KH, Parlow AF & Simpson ER 1998 Characterization of mice deficient in aromatase (Ar KO) because of targeted disruption of the cyp19 gene. PNAS 95 6965-6970. (doi:10.1073/pnas.95.12.6965)
42. Fleming N. I, Knower KC, Lazarus KA, Fuller PJ, Simpson ER & Clyne CD 2010 Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter. PLoS ONE 5 e14389. (doi:10.1371/journal.pone.0014389)
43. Garcia-Ortiz J. E, Pelosi E, Omari S, Nedorezov T, Piao Y, Karmazin J, Uda M, Cao A., Cole SW, Forabosco A et al. 2009 Foxl2 functions in sex determination and histogenesis throughout mouse ovary development. BMC Developmental Biology 9 36. (doi:10.1186/1471-213X-9-36)
44. Georges A., Benayoun BA, Marongiu M, Dipietromaria A, L'Hôte D, Todeschini A.-L, Auer J, Crisponi L & Veitia RA 2011 SUMOylation of the forkhead transcription factor FOXL2 promotes its stabilization/ activation through transient recruitment to PML bodies. PLoS ONE 6 e25463. (doi:10.1371/journal.pone.0025463)
45. Ghochani Y., Saini JK, Mellon PL & Thackray VG 2012 FOXL2 is involved in the synergy between activin and progestins on the follicle-stimulating hormone b-subunit promoter. Endocrinology 153 2023-2033. (doi:10. 1210/en.2011-1763)
46. Hiramatsu R., Harikae K, Tsunekawa N, Kurohmaru M, Matsuo I & Kanai Y 2010 FGF signaling directs a center-to-pole expansion of tubulogenesis in mouse testis differentiation. Development 137 303-312. (doi:10. 1242/dev.040519)
47. Huang E. J, Manova K, Packer AI, Sanchez S, Bachvarova RF & Besmer P 1993 The murine steel panda mutation affects Kit ligand expression and growth of early ovarian follicles. Developmental Biology 157 100-109. (doi:10.1006/dbio.1993.1115)
48. Jamieson S. & Fuller PJ 2012 Molecular pathogenesis of granulosa cell tumors of the ovary. Endocrine Reviews 33 109-144. (doi:10.1210/er. 2011-0014)
49. Jamieson S., Butzow R, Andersson N, Alexiadis M, Unkila-Kallio L, Heikinheimo M., Fuller PJ & Anttonen M 2010 The FOXL2 C134W mutation is characteristic of adult granulosa cell tumors of the ovary. Modern Pathology 23 1477-1485. (doi:10.1038/modpathol.2010.145)
50. John G. B, Gallardo TD, Shirley LJ & Castrillon DH 2008 Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Developmental Biology 321 197-204. (doi:10.1016/ j.ydbio.2008.06.017)
51. Jorgez C. J, Klysik M, Jamin SP, Behringer RR & Matzuk MM 2004 Granulosa cell-specific inactivation of follistatin causes female fertility defects. Molecular Endocrinology 18 953-967. (doi:10.1210/me.2003-0301)
52. Justice N. J, Blount AL, Pelosi E, Schlessinger D, Vale W & Bilezikjian LM 2011 Impaired FSHb expression in the pituitaries of Foxl2 mutant animals. Molecular Endocrinology 25 1404-1415. (doi:10.1210/ me.2011-0093)
53. Kalfa N., Philibert P, Patte C, Ecochard A, Duvillard P, Baldet P, Jaubert F, Fellous M. & Sultan C 2007 Extinction of FOXL2 expression in aggressive ovarian granulosa cell tumors in children. Fertility and Sterility 87 896-901. (doi:10.1016/j.fertnstert.2006.11.016)
54. Kashimada K., Pelosi E, Chen H, Schlessinger D, Wilhelm D & Koopman P 2011 FOXL2 and BMP2 act cooperatively to regulate follistatin gene expression during ovarian development. Endocrinology 152 272-280. (doi:10.1210/en.2010-0636)
55. Kezele P., Nilsson EE & Skinner MK 2005 Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biology of Reproduction 73 967-973. (doi:10.1095/ biolreprod.105.043117)
56. Kim S.-Y, Weiss J, Tong M, Laronda MM, Lee E-J & Jameson JL 2009 Foxl2, a forkhead transcription factor, modulates nonclassical activity of the estrogen receptor-a. Endocrinology 150 5085-5093. (doi:10.1210/en. 2009-0313)
57. Kim J.-H, Yoon S, Park M, Park H-O, Ko J-J, Lee K & Bae J 2011 Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (C134W). Oncogene 30 1653-1663. (doi:10.1038/onc.2010.541)
58. Kuo F.-T, Bentsi-Barnes IK, Barlow GM, Bae J & Pisarska MD 2009 Sumoylation of forkhead L2 by Ubc9 is required for its activity as a transcriptional repressor of the steroidogenic acute regulatory gene. Cellular Signalling 21 1935-1944. (doi:10.1016/j.cellsig.2009.09.001)
59. Kuo F.-T, Bentsi-Barnes IK, Barlow GM & Pisarska MD 2011 Mutant forkhead L2 (FOXL2) proteins associated with premature ovarian failure (POF) dimerize with wild-type FOXL2, leading to altered regulation of genes associated with granulosa cell differentiation. Endocrinology 152 3917-3929. (doi:10.1210/en.2010-0989)
60. Lakhal B., Ben-Hadj-Khalifa S, Bouali N, Philipert P, Audran F, Braham R, Hatem E., Sultan C & Saad A 2012 Mutational screening of SF1 and WNT4 in Tunisian women with premature ovarian failure. Gene 509 298-301. (doi:10.1016/j.gene.2012.08.007)
61. Lamba P., Fortin J, Tran S, Wang Y & Bernard DJ 2009 A novel role for the forkhead transcription factor FOXL2 in activin A-regulated folliclestimulating hormone b subunit transcription. Molecular Endocrinology 23 1001-1013. (doi:10.1210/me.2008-0324)
62. Lamba P., Wang Y, Tran S, Ouspenskaia T, Libasci V, Hébert TE, Miller GJ & Bernard D. J 2010 Activin A regulates porcine follicle-stimulating hormone b-subunit transcription via cooperative actions of SMADs and FOXL2. Endocrinology 151 5456-5467. (doi:10.1210/en.2010-0605)
63. Lan C.-W, Chen M-J, Jan P-S, Chen H-F & Ho H-N 2013 Differentiation of human embryonic stem cells into functional ovarian granulosa-like cells. Journal of Clinical Endocrinology and Metabolism 98 3713-3723. (doi:10.1210/jc.2012-4302)
64. Lee W.-S, Otsuka F, Moore RK & Shimasaki S 2001 Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biology of Reproduction 65 994-999. (doi:10.1095/biolreprod65.4.994)
65. Lee M. B, Lebedeva LA, Suzawa M, Wadekar SA, Desclozeaux M & Ingraham H. A 2005a The DEAD-box protein DP103 (Ddx20 or Gemin-3) represses orphan nuclear receptor activity via SUMO modification. Molecular and Cellular Biology 25 1879-1890. (doi:10.1128/MCB.25.5.1879-1890.2005)
66. Lee C. S, Friedman JR, Fulmer JT & Kaestner KH 2005b The initiation of liver development is dependent on Foxa transcription factors. Nature 435 944-947. (doi:10.1038/nature03649)
67. L'Hôte D, Georges A, Todeschini AL, Kim J-H, Benayoun BA, Bae J & Veitia RA 2012 Discovery of novel protein partners of the transcription factor FOXL2 provides insights into its physiopathological roles. Human Molecular Genetics 21 3264-3274. (doi:10.1093/hmg/dds170)
68. Lima J. F, Jin L, de Araujo ARC, Erikson-Johnson MR, Oliveira AM, Sebo TJ, Keeney G. L & Medeiros F 2012 FOXL2 mutations in granulosa cell tumors occurring in males. Archives of Pathology & Laboratory Medicine 136 825-828. (doi:10.5858/arpa.2011-0355-OA)
69. Liu C.-F, Bingham N, Parker K & Yao HH-C 2009 Sex-specific roles of b-catenin in mouse gonadal development. Human Molecular Genetics 18 405-417. (doi:10.1093/hmg/ddn362)
70. Liu A. M, Wong K-F, Jiang X, Qiao Y & Luk JM 2012 Regulators of mammalian Hippo pathway in cancer. Biochimica et Biophysica Acta 1826 357-364. (doi:10.1016/j.bbcan.2012.05.006)
71. Maatouk D. M, DiNapoli L, Alvers A, Parker KL, Taketo MM & Capel B 2008 Stabilization of b-catenin in XY gonads causes male-to-female sex-reversal. Human Molecular Genetics 17 2949-2955. (doi:10.1093/ hmg/ddn193)
72. Manuylov N. L, Smagulova FO, Leach L & Tevosian SG 2008 Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 135 3731-3743. (doi:10.1242/dev.024653)
73. Marongiu M., Deiana M, Meloni A, Marcia L, Puddu A, Cao A, Schlessinger D. & Crisponi L 2010 The forkhead transcription factor Foxl2 is sumoylated in both human and mouse: sumoylation affects its stability, localization, and activity. PLoS ONE 5 e9477. (doi:10.1371/journal.pone.0009477)
74. Matson C. K, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ & Zarkower D. 2011 DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476 101-104. (doi:10.1038/ nature10239)
75. Matzuk M. M, Finegold MJ, Su JG, Hsueh AJ & Bradley A 1992 a-Inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360 313-319. (doi:10.1038/360313a0)
76. McCue PM, Roser JF, Munro CJ, Liu IKM & Lasley BL 2006 Granulosa cell tumors of the equine ovary. Veterinary Clinics of North America. Equine Practice 22 799-817. (doi:10.1016/j.cveq.2006.08.008)
77. McTavish KJ, Nonis D, Hoang YD & Shimasaki S 2013 Granulosa cell tumor mutant FOXL2C134W suppresses GDF-9 and activin A-induced follistatin transcription in primary granulosa cells. Molecular and Cellular Endocrinology 372 57-64. (doi:10.1016/j.mce.2013.03.021)
78. Miyamoto Y., Taniguchi H, Hamel F, Silversides DW & Viger RS 2008 A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Molecular Biology 9 44. (doi:10.1186/1471-2199-9-44)
79. Moumné L, Dipietromaria A, Batista F, Kocer A, Fellous M, Pailhoux E & Veitia R. A 2008 Differential aggregation and functional impairment induced by polyalanine expansions in FOXL2, a transcription factor involved in cranio-facial and ovarian development. Human Molecular Genetics 17 1010-1019. (doi:10.1093/hmg/ddm373)
80. Nilsson E. E & Skinner MK 2003 Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biology of Reproduction 69 1265-1272. (doi:10.1095/ biolreprod.103.018671)
81. Nilsson E. E & Skinner MK 2004 Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Molecular and Cellular Endocrinology 214 19-25. (doi:10. 1016/j.mce.2003.12.001)
82. Nilsson E. E, Kezele P & Skinner MK 2002 Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Molecular and Cellular Endocrinology 188 65-73. (doi:10.1016/S0303-7207(01)00746-8)
83. Nilsson E., Rogers N & Skinner MK 2007 Actions of anti-Müllerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 134 209-221. (doi:10.1530/ REP-07-0119)
84. Nonis D., McTavish KJ & Shimasaki S 2013 Essential but differential role of FOXL2wt and FOXL2C134W in GDF-9 stimulation of follistatin transcription in co-operation with Smad3 in the human granulosa cell line COV434. Molecular and Cellular Endocrinology 372 42-48. (doi:10.1016/ j.mce.2013.02.020)
85. Ohishi Y., Oda Y, Kurihara S, Kaku T, Kobayashi H, Wake N & Tsuneyoshi M 2011 Nuclear localization of E-cadherin but not b-catenin in human ovarian granulosa cell tumours and normal ovarian follicles and ovarian stroma. Histopathology 58 423-432. (doi:10.1111/j.1365-2559. 2011.03761.x)
86. Ohkura N., Kitagawa Y & Sakaguchi S 2013 Development and maintenance of regulatory T cells. Immunity 38 414-423. (doi:10.1016/j.immuni. 2013.03.002)
87. Pailhoux E., Vigier B, Schibler L, Cribiu EP, Cotinot C & Vaiman D 2005 Positional cloning of the PIS mutation in goats and its impact on understanding mammalian sex-differentiation. Genetics, Selection, Evolution 37 (Suppl 1) S55-S64. (doi:10.1186/1297-9686-37-S1-S55)
88. Pangas S. A, Choi Y, Ballow DJ, Zhao Y, Westphal H, Matzuk MM & Rajkovic A. 2006 Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. PNAS 103 8090-8095. (doi:10.1073/pnas. 0601083103)
89. Pangas S. A, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin J. F, Jamin SP, Behringer RR et al. 2008 Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Molecular and Cellular Biology 28 248-257. (doi:10.1128/MCB.01404-07)
90. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pepin B, Cotinot C., Veitia R & Pailhoux E 2006 FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. Journal of Molecular Endocrinology 36 399-413. (doi:10.1677/jme.1.01947)
91. Paredes A., Romero C, Dissen GA, DeChiara TM, Reichardt L, Cornea A, Ojeda S. R & Xu B 2004 TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. Developmental Biology 267 430-449. (doi:10.1016/j.ydbio.2003.12.001)
92. Park M., Shin E, Won M, Kim J-H, Go H, Kim H-L, Ko J-J, Lee K & Bae J 2010 FOXL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1-induced CYP17 transcription in granulosa cells. Molecular Endocrinology 24 1024-1036. (doi:10.1210/me.2009-0375)
93. Parrott J. A & Skinner MK 1999 Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140 4262-4271. (doi:10.1210/en.140.9.4262)
94. Pisarska M. D, Bae J, Klein C & Hsueh AJW 2004 Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 145 3424-3433. (doi:10.1210/ en.2003-1141)
95. Pisarska M. D, Kuo F-T, Bentsi-Barnes IK, Khan S & Barlow GM 2010 LATS1 phosphorylates forkhead L2 and regulates its transcriptional activity. American Journal of Physiology. Endocrinology and Metabolism 299 E101-E109. (doi:10.1152/ajpendo.00534.2009)
96. Pisarska M. D, Barlow G & Kuo F-T 2011 Minireview: roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology 152 1199-1208. (doi:10.1210/en.2010-1041)
97. Poznic M 2009 Retinoblastoma protein: a central processing unit. Journal of Biosciences 34 305-312. (doi:10.1007/s12038-009-0034-2)
98. Qin Y., Choi Y, Zhao H, Simpson JL, Chen Z-J & Rajkovic A 2007 NOBOX homeobox mutation causes premature ovarian failure. American Journal of Human Genetics 81 576-581. (doi:10.1086/519496)
99. Rajareddy S., Reddy P, Du C, Liu L, Jagarlamudi K, Tang W, Shen Y, Berthet C, Peng S. L, Kaldis P et al. 2007 p27kip1 (cyclin-dependent kinase inhibitor 1B) controls ovarian development by suppressing follicle endowment and activation and promoting follicle atresia in mice. Molecular Endocrinology 21 2189-2202. (doi:10.1210/me.2007-0172)
100. Rajkovic A., Pangas SA, Ballow D, Suzumori N & Matzuk MM 2004 NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305 1157-1159. (doi:10.1126/science.1099755)
101. Reddy P., Shen L, Ren C, Boman K, Lundin E, Ottander U, Lindgren P, LiuY-X, Sun Q.-Y & Liu K 2005 Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Developmental Biology 281 160-170. (doi:10.1016/j.ydbio.2005.02.013)
102. Reddy P., Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hämäläinen T, Peng SL et al. 2008 Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319 611-613. (doi:10.1126/science.1152257)
103. Richards J. S, Fan H-Y, Liu Z, Tsoi M, Laguë M-N, Boyer A & Boerboom D 2012 Either Kras activation or Pten loss similarly enhance the dominant-stable CTNNB1-induced genetic program to promote granulosa cell tumor development in the ovary and testis. Oncogene 31 1504-1520. (doi:10.1038/onc.2011.341)
104. Risma K. A, Clay CM, Nett TM, Wagner T, Yun J & Nilson JH 1995 Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors. PNAS 92 1322-1326. (doi:10.1073/pnas.92.5.1322)
105. Rosario R., Araki H, Print CG & Shelling AN 2012 The transcriptional targets of mutant FOXL2 in granulosa cell tumours. PLoS ONE 7 e46270. (doi:10.1371/journal.pone.0046270)
106. Rosario R., Blenkiron C & Shelling AN 2013 Comparative study of microRNA regulation on FOXL2 between adult-type and juvenile-type granulosa cell tumours in vitro. Gynecologic Oncology 129 209-215. (doi:10.1016/j.ygyno.2012.12.034)
107. Schmidt D., Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier A-C & Treier M. 2004 The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131 933-942. (doi:10.1242/dev.00969)
108. Shah S. P, Köbel M, Senz J, Morin RD, Clarke BA, Wiegand KC, Leung G, Zayed A., Mehl E, Kalloger SE et al. 2009 Mutation of FOXL2 in granulosa-cell tumors of the ovary. New England Journal of Medicine 360 2719-2729. (doi:10.1056/NEJMoa0902542)
109. Steinmetz R., Wagoner HA, Zeng P, Hammond JR, Hannon TS, Meyers JL & Pescovitz O. H 2004 Mechanisms regulating the constitutive activation of the extracellular signal-regulated kinase (ERK) signaling pathway in ovarian cancer and the effect of ribonucleic acid interference for ERK1/2 on cancer cell proliferation. Molecular Endocrinology 18 2570-2582. (doi:10.1210/me.2004-0082)
110. St John M. A, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow A. F, McGrath J & Xu T 1999 Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nature Genetics 21 182-186. (doi:10.1038/5965)
111. Tavassoli F. A & Devilee P (Eds) 2003 World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Breast and Female Genital Organs. Lyon: IARC Press.
112. Todeschini A.-L, Dipietromaria A, L'Hôte D, Boucham FZ, Georges AB, Pandaranayaka P. JE, Krishnaswamy S, Rivals I, Bazin C & Veitia RA 2011 Mutational probing of the forkhead domain of the transcription factor FOXL2 provides insights into the pathogenicity of naturally occurring mutations. Human Molecular Genetics 20 3376-3385. (doi:10.1093/ hmg/ddr244)
113. Tran S., Lamba P, Wang Y & Bernard DJ 2011 SMADs and FOXL2 synergistically regulate murine FSHb transcription via a conserved proximal promoter element. Molecular Endocrinology 25 1170-1183. (doi:10.1210/me.2010-0480)
114. Tran S., Zhou X, Lafleur C, Calderon MJ, Ellsworth BS, Kimmins S, Boehm U, Treier M., Boerboom D & Bernard DJ 2013 Impaired fertility and FSH synthesis in gonadotrope-specific Foxl2 knockout mice. Molecular Endocrinology 27 407-421. (doi:10.1210/me.2012-1286)
115. Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, Kimber W, Forabosco A, Cao A., Schlessinger D & Pilia G 2004 Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Human Molecular Genetics 13 1171-1181. (doi:10.1093/hmg/ddh124)
116. Uhlenhaut N. H, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier A-C, Klugmann C., Klasen C, Holter NI et al. 2009 Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139 1130-1142. (doi:10.1016/j.cell.2009.11.021)
117. Vainio S., Heikkilä M, Kispert A, Chin N & McMahon AP 1999 Female development in mammals is regulated by Wnt-4 signalling. Nature 397 405-409. (doi:10.1038/17068)
118. Van der Vos KE & Coffer PJ 2008 FOXO-binding partners: it takes two to tango. Oncogene 27 2289-2299. (doi:10.1038/onc.2008.22)
119. Verdin H. & De Baere E 2012 FOXL2 impairment in human disease. Hormone Research in Paediatrics 77 2-11. (doi:10.1159/000335236)
120. Vidal V. P, Chaboissier MC, de Rooij DG & Schedl A 2001 Sox9 induces testis development in XX transgenic mice. Nature Genetics 28 216-217. (doi:10.1038/90046)
121. Watson R. H, Roy WJ Jr, Davis M, Hitchcock A & Campbell IG 1997 Loss of heterozygosity at the a-inhibin locus on chromosome 2q is not a feature of human granulosa cell tumors. Gynecologic Oncology 65 387-390. (doi:10.1006/gyno.1997.4682)
122. Woods D. C, White YAR, Niikura Y, Kiatpongsan S, Lee H-J & Tilly JL 2013 Embryonic stem cell-derived granulosa cells participate in ovarian follicle formation in vitro and in vivo. Reproductive Sciences 20 524-535. (doi:10.1177/1933719113483017)
123. Yao H. H-C, Whoriskey W & Capel B 2002 Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes and Development 16 1433-1440. (doi:10.1101/gad.981202)
124. Yao H. HC, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A & Capel B 2004 Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Developmental Dynamics 230 210-215. (doi:10.1002/ dvdy.20042)
125. Yoshida H., Takakura N, Kataoka H, Kunisada T, Okamura H & Nishikawa SI 1997 Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Developmental Biology 184 122-137. (doi:10.1006/ dbio.1997.8503)
126. Zaret K. S & Carroll JS 2011 Pioneer transcription factors: establishing competence for gene expression. Genes and Development 25 2227-2241. (doi:10.1101/gad.176826.111)