FOXL2 impairment in human disease

Hormone Research in Paediatrics

Volumn 77, Issue 1, 2012, Pages 2-11

  Verdin, Hannah ^a   De Baere, Elfride ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Adult GCT; Anti testis action; BPES; FOXL2 mutation; POF

Indexed keywords

BLEPHAROPHIMOSIS; CELL TRANSDIFFERENTIATION; CONFERENCE PAPER; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; FOXL 2 GENE; GENE; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENETIC DISORDER; GENOTYPE PHENOTYPE CORRELATION; GOAT; GRANULOSA CELL TUMOR; HUMAN; KNOCKOUT MOUSE; MOLECULAR PATHOLOGY; NEOPLASM; NONHUMAN; PHENOTYPE; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; SOMATIC MUTATION;

ANIMALS; BLEPHAROPHIMOSIS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GENETIC TESTING; GRANULOSA CELL TUMOR; HUMANS; OVARIAN NEOPLASMS; PRIMARY OVARIAN INSUFFICIENCY;

EID: 84857358698     PISSN: 16632818     EISSN: 16632826     Source Type: Journal    
DOI: 10.1159/000335236     Document Type: Conference Paper

References (66)

1. Lehmann OJ, Sowden JC, Carlsson P, Jordan T, Bhattacharya SS: Fox's in development and disease. Trends Genet 2003; 19: 339-344. (Pubitemid 36694617)
2. 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. (Pubitemid 32157442)
3. 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.
4. 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. (Pubitemid 38064899)
5. Treier M, Gleiberman AS, O'Connell SM, Szeto DP, McMahon JA, McMahon AP, Rosenfeld MG: Multistep signaling requirements for pituitary organogenesis in vivo. Genes Dev 1998; 12: 1691-1704. (Pubitemid 28299519)
6. 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. (Pubitemid 44833536)
7. Decock CE, Claerhout I, Leroy BP, Kesteleyn P, Shah AD, De Baere E: Correction of the lower eyelid malpositioning in the blepharophimosis-ptosis- epicanthus inversus syndrome. Ophthal Plast Reconstr Surg 2011; 27: 368-370.
8. Oley C, Baraitser M: Blepharophimosis, ptosis, epicanthus inversus syndrome (BPES syndrome). J Med Genet 1988; 25: 47-51. (Pubitemid 18042303)
9. Zlotogora J, Sagi M, Cohen T: The blepharophimosis, ptosis, and epicanthus inversus syndrome: Delineation of two types. Am J Hum Genet 1983; 35: 1020-1027. (Pubitemid 13008598)
10. De Vos M, Devroey P, Fauser BC: Primary ovarian insufficiency. Lancet 2010; 376: 911-921.
11. Fraser IS, Shearman RP, Smith A, Russell P: An association among blepharophimosis, resistant ovary syndrome, and true premature menopause. Fertil Steril 1988; 50: 747-751.
12. Meduri G, Bachelot A, Duflos C, Bstandig B, Poirot C, Genestie C, Veitia R, De Baere E, Touraine P: FOXL2 mutations lead to different ovarian phenotypes in BPES patients: Case report. Hum Reprod 2010; 25: 235-243.
13. Goswami D, Conway GS: Premature ovarian failure. Hum Reprod Update 2005; 11: 391-410. (Pubitemid 40895467)
14. Kalantaridou SN, Davis SR, Nelson LM: Premature ovarian failure. Endocrinol Metab Clin North Am 1998; 27: 989-1006. (Pubitemid 28564068)
15. Donnez J, Dolmans MM: Preservation of fertility in females with haematological malignancy. Br J Haematol 2011; 154: 175-184.
16. Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM: Ovarian tissue cryopreservation and transplantation: A review. Hum Reprod Update 2006; 12: 519-535. (Pubitemid 44288709)
17. Tao T, Del Valle A: Human oocyte and ovarian tissue cryopreservation and its application. J Assist Reprod Genet 2008; 25: 287-296.
18. Cobo A, Remohi J, Chang CC, Nagy ZP: Oocyte cryopreservation for donor egg banking. Reprod Biomed Online 2011; 23: 341-346.
19. Beysen D, De Paepe A, Baere ED: FOXL2 mutations and genomic rearrangements in BPES. Hum Mutat 2009; 30: 158-169.
20. De Baere E, Beysen D, Oley C, et al: FOXL2 and BPES: Mutational hotspots, phenotypic variability, and revision of the genotypephenotype correlation. Am J Hum Genet 2003; 72: 478-487. (Pubitemid 36194256)
21. De Baere E, Dixon MJ, Small KW, et al: Spectrum of FOXL2 gene mutations in blepharophimosis-ptosis-epicanthus inversus (BPES) families demonstrate a genotype-phenotype correlation. Hum Mol Genet 2001; 10: 1591-1600. (Pubitemid 32734311)
22. Caburet S, Demarez A, Moumne L, Fellous M, De Baere E, Veitia RA: A recurrent polyalanine expansion in the transcription factor FOXL2 induces extensive nuclear and cytoplasmic protein aggregation. J Med Genet 2004; 41: 932-936. (Pubitemid 40007254)
23. Moumne L, Dipietromaria A, Batista F, Kocer A, Fellous M, Pailhoux E, Veitia RA: Differential aggregation and functional impairment induced by polyalanine expansions in FOXL2, a transcription factor involved in cranio-facial and ovarian development. Hum Mol Genet 2008; 17: 1010-1019. (Pubitemid 351426035)
24. Beysen D, Moumne L, Veitia R, Peters H, Leroy BP, De Paepe A, De Baere E: Missense mutations in the forkhead domain of FOXL2 lead to subcellular mislocalization, protein aggregation and impaired transactivation. Hum Mol Genet 2008; 17: 2030-2038. (Pubitemid 351865851)
25. Dipietromaria A, Benayoun BA, Todeschini AL, Rivals I, Bazin C, Veitia RA: Towards a functional classification of pathogenic FOXL2 mutations using transactivation reporter systems. Hum Mol Genet 2009; 18: 3324-3333.
26. Todeschini AL, Dipietromaria A, L'Hote D, Boucham FZ, Georges AB, Pandaranayaka PJ, Krishnaswamy S, Rivals I, Bazin C, Veitia RA: Mutational probing of the forkhead domain of the transcription factor FOXL2 provides insights into the pathogenicity of naturally occurring mutations. Hum Mol Genet 2011; 20: 3376-3385.
27. Beysen D, Raes J, Leroy BP, et al: Deletions involving long-range conserved nongenic sequences upstream and downstream of FOXL2 as a novel disease-causing mechanism in blepharophimosis syndrome. Am J Hum Genet 2005; 77: 205-218. (Pubitemid 41022704)
28. D'haene B, Nevado J, Pugeat M, et al: FOXL2 copy number changes in the molecular pathogenesis of BPES: Unique cohort of 17 deletions. Hum Mutat 2010; 31:E1332-E1347.
29. Crisponi L, Uda M, Deiana M, Loi A, Nagaraja R, Chiappe F, Schlessinger D, Cao A, Pilia G: FOXL2 inactivation by a translocation 171 kb away: Analysis of 500 kb of chromosome for candidate long-range regulatory sequences. Genomics 2004; 83: 757-764. (Pubitemid 38469918)
30. D'Haene B, Attanasio C, Beysen D, Dostie J, Lemire E, Bouchard P, Field M, Jones K, Lorenz B, Menten B, Buysse K, Pattyn F, Friedli M, Ucla C, Rossier C, Wyss C, Speleman F, De Paepe A, Dekker J, Antonarakis SE, De Baere E: Disease-causing 7.4 kb cisregulatory deletion disrupting conserved non-coding sequences and their interaction with the FOXL2 promotor: Implications for mutation screening. PLoS Genet 2009; 5:e1000522.
31. Li WX, Wang XK, Sun Y, Wang YL, Lin LX, Tang SJ: A novel mutation in the FOXL2 gene in a Chinese family with blepharophimosis, ptosis, and epicanthus inversus syndrome. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2005; 22: 372-375. (Pubitemid 41153461)
32. Qian X, Shu A, Qin W, Xing Q, Gao J, Yang J, Feng G, He L: A novel insertion mutation in the FOXL2 gene is detected in a big Chinese family with blepharophimosis-ptosisepicanthus inversus. Mutat Res 2004; 554: 19-22. (Pubitemid 39140811)
33. Gijsbers AC, D'Haene B, Hilhorst-Hofstee Y, Mannens M, Albrecht B, Seidel J, Witt DR, Maisenbacher MK, Loeys B, van Essen T, Bakker E, Hennekam R, Breuning MH, De Baere E, Ruivenkamp CA: Identification of copy number variants associated with BPES-like phenotypes. Hum Genet 2008; 124: 489-498.
34. De Baere E, Lemercier B, Christin-Maitre S, Durval D, Messiaen L, Fellous M, Veitia R: FOXL2 mutation screening in a large panel of POF patients and XX males. J Med Genet 2002; 39:e43.
35. Harris SE, Chand AL, Winship IM, Gersak K, Aittomaki K, Shelling AN: Identification of novel mutations in FOXL2 associated with premature ovarian failure. Mol Hum Reprod 2002; 8: 729-733.
36. Bodega B, Porta C, Crosignani PG, Ginelli E, Marozzi A: Mutations in the coding region of the FOXL2 gene are not a major cause of idiopathic premature ovarian failure. Mol Hum Reprod 2004; 10: 555-557. (Pubitemid 39136813)
37. Ni F, Wen Q, Wang B, Zhou S, Wang J, Mu Y, Ma X, Cao Y: Mutation analysis of FOXL2 gene in Chinese patients with premature ovarian failure. Gynecol Endocrinol 2010; 26: 246-249.
38. Laissue P, Lakhal B, Benayoun BA, Dipietromaria A, Braham R, Elghezal H, Philibert P, Saad A, Sultan C, Fellous M, Veitia RA: Functional evidence implicating FOXL2 in non-syndromic premature ovarian failure and in the regulation of the transcription factor OSR2. J Med Genet 2009; 46: 455-457.
39. Gersak K, Harris SE, Smale WJ, Shelling AN: A novel 30 bp deletion in the foxl2 gene in a phenotypically normal woman with primary amenorrhoea: Case report. Hum Reprod 2004; 19: 2767-2770. (Pubitemid 40028945)
40. Chatterjee S, Modi D, Maitra A, Kadam S, Patel Z, Gokrall J, Meherji P: Screening for FOXL2 gene mutations in women with premature ovarian failure: An Indian experience. Reprod Biomed Online 2007; 15: 554-560. (Pubitemid 350167078)
41. Geetha P, Nair MK: Granulosa cell tumours of the ovary. Aust NZ J Obstet Gynaecol 2010; 50: 216-220.
42. Schumer ST, Cannistra SA: Granulosa cell tumor of the ovary. J Clin Oncol 2003; 21: 1180-1189. (Pubitemid 46594151)
43. Shah SP, Kobel M, Senz J, et al: Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med 2009; 360: 2719-2729.
44. Benayoun BA, Caburet S, Dipietromaria A, Georges A, D'Haene B, Pandaranayaka PJ, L'Hote D, Todeschini AL, Krishnaswamy S, Fellous M, De Baere E, Veitia RA: Functional exploration of the adult ovarian granulosa cell tumor-associated somatic FOXL2 mutation p.Cys134trp (c.402c 1 g). PLoS One 2010; 5:e8789.
45. Schrader KA, Gorbatcheva B, Senz J, Heravi-Moussavi A, Melnyk N, Salamanca C, Maines-Bandiera S, Cooke SL, Leung P, Brenton JD, Gilks CB, Monahan J, Huntsman DG: The specificity of the FOXL2 c.402c 1 g somatic mutation: A survey of solid tumors. PLoS One 2009; 4:e7988.
46. Jamieson S, Butzow R, Andersson N, Alexiadis M, Unkila-Kallio L, Heikinheimo M, Fuller PJ, Anttonen M: The FOXL2 c134w mutation is characteristic of adult granulosa cell tumors of the ovary. Mod Pathol 2010; 23: 1477-1485.
47. Kim JH, Yoon S, Park M, Park HO, Ko JJ, Lee K, Bae J: Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (c134w). Oncogene 2011; 30: 1653-1663.
48. Kim MS, Hur SY, Yoo NJ, Lee SH: Mutational analysis of FOXL2 codon 134 in granulosa cell tumour of ovary and other human cancers. J Pathol 2010; 221: 147-152.
49. Hes O, Vanecek T, Petersson F, Grossmann P, Hora M, Perez Montiel DM, Steiner P, Dvorak M, Michal M: Mutational analysis (c.402c 1 g) of the FOXL2 gene and immunohistochemical expression of the FOXL2 protein in testicular adult type granulosa cell tumors and incompletely differentiated sex cord stromal tumors. Appl Immunohistochem Mol Morphol 2011; 19: 347-351.
50. Al-Agha OM, Huwait HF, Chow C, Yang W, Senz J, Kalloger SE, Huntsman DG, Young RH, Gilks CB: FOXL2 is a sensitive and specific marker for sex cord-stromal tumors of the ovary. Am J Surg Pathol 2011; 35: 484-494.
51. D'Angelo E, Mozos A, Nakayama D, Espinosa I, Catasus L, Munoz J, Prat J: Prognostic significance of FOXL2 mutation and mRNA expression in adult and juvenile granulosa cell tumors of the ovary. Mod Pathol 2011; 24: 1360-1367.
52. Gershon R, Aviel-Ronen S, Korach J, Daniel-Carmi V, Avivi C, Bar-Ilan D, Barshack I, Meirow D, Ben-Baruch G, Cohen Y: FOXL2 C402G mutation detection using MALDITOF-MS in DNA extracted from Israeli granulosa cell tumors. Gynecol Oncol 2011; 122: 580-584.
53. Fleming NI, Knower KC, Lazarus KA, Fuller PJ, Simpson ER, Clyne CD: 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 2010; 5:e14389.
54. Benayoun BA, Georges AB, L'Hote D, Andersson N, Dipietromaria A, Todeschini AL, Caburet S, Bazin C, Anttonen M, Veitia RA: Transcription factor FOXL2 protects granulosa cells from stress and delays cell cycle: Role of its regulation by the SIRT1 deacetylase. Hum Mol Genet 2011; 20: 1673-1686.
55. 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. (Pubitemid 38263207)
56. Uda M, Ottolenghi C, Crisponi L, Garcia JE, Deiana M, Kimber W, Forabosco A, Cao A, Schlessinger D, Pilia G: FOXL2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum Mol Genet 2004; 13: 1171-1181. (Pubitemid 38786999)
57. Pailhoux E, Vigier B, Chaffaux S, Servel N, Taourit S, Furet JP, Fellous M, Grosclaude F, Cribiu EP, Cotinot C, Vaiman D: A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat Genet 2001; 29: 453-458. (Pubitemid 34326697)
58. Ottolenghi C, Omari S, Garcia-Ortiz JE, Uda M, Crisponi L, Forabosco A, Pilia G, Schlessinger D: FOXL2 is required for commitment to ovary differentiation. Hum Mol Genet 2005; 14: 2053-2062. (Pubitemid 41418041)
59. Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D: Loss of WNT4 and FOXL2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 2007; 16: 2795-2804. (Pubitemid 350048379)
60. 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 reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009; 139: 1130-1142.
61. Murphy BD: Revisiting reproduction: What a difference a gene makes. Nat Med 2010; 16: 527-529.
62. Kaur I, Hussain A, Naik MN, Murthy R, Honavar SG: Mutation spectrum of fork-head transcriptional factor gene (FOXL2) in Indian blepharophimosis ptosis epicanthus inversus syndrome (BPES) patients. Br J Ophthalmol 2011; 95: 881-886.
63. Goodarzi MO, Dumesic DA, Chazenbalk G, Azziz R: Polycystic ovary syndrome: Etiology, pathogenesis and diagnosis. Nat Rev Endocrinol 2011; 7: 219-231.
64. Rodin DA, Bano G, Bland JM, Taylor K, Nussey SS: Polycystic ovaries and associated metabolic abnormalities in Indian subcontinent Asian women. Clin Endocrinol (Oxf) 1998; 49: 91-99. (Pubitemid 28338048)
65. Marneros AG, Krieg T: Keloids-clinical diagnosis, pathogenesis, and treatment options. J German Soc Dermatol JDDG 2004; 2: 905-913. (Pubitemid 39472352)
66. Nakashima M, Chung S, Takahashi A, Kamatani N, Kawaguchi T, Tsunoda T, Hosono N, Kubo M, Nakamura Y, Zembutsu H: A genome-wide association study identifies four susceptibility loci for keloid in the Japanese population. Nat Genet 2010; 42: 768-771.